Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2015 (2015), Article ID 509306, 13 pages
http://dx.doi.org/10.1155/2015/509306
Review Article

Dengue Virus-Induced Inflammation of the Endothelium and the Potential Roles of Sphingosine Kinase-1 and MicroRNAs

1Microbiology and Infectious Diseases, School of Medicine, Flinders University, Bedford Park, Adelaide, SA 5042, Australia
2Centre for Cancer Biology, University of South Australia and SA Pathology, Adelaide, SA 5000, Australia

Received 10 July 2015; Revised 2 October 2015; Accepted 8 October 2015

Academic Editor: Caio T. Fagundes

Copyright © 2015 Amanda L. Aloia 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. J. S. Pober and W. C. Sessa, “Evolving functions of endothelial cells in inflammation,” Nature Reviews Immunology, vol. 7, no. 10, pp. 803–815, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. S. B. Halstead, “Antibody, macrophages, dengue virus infection, shock, and hemorrhage: a pathogenetic cascade,” Reviews of Infectious Diseases, vol. 11, supplement 4, pp. S830–S839, 1989. View at Publisher · View at Google Scholar · View at Scopus
  3. S. B. Halstead, “Dengue,” The Lancet, vol. 370, no. 9599, pp. 1644–1652, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. C. P. Simmons, J. J. Farrar, N. V. V. Chau, and B. Wills, “Current concepts: dengue,” The New England Journal of Medicine, vol. 366, no. 15, pp. 1423–1432, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. M. G. Guzman, S. B. Halstead, H. Artsob et al., “Dengue: a continuing global threat,” Nature Reviews Microbiology, vol. 8, supplement 12, pp. S7–S16, 2010. View at Google Scholar
  6. V. V. Costa, C. T. Fagundes, D. G. Souza, and M. M. Teixeira, “Inflammatory and innate immune responses in dengue infection: protection versus disease induction,” The American Journal of Pathology, vol. 182, no. 6, pp. 1950–1961, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Basu and U. C. Chaturvedi, “Vascular endothelium: the battlefield of dengue viruses,” FEMS Immunology and Medical Microbiology, vol. 53, no. 3, pp. 287–299, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. N. A. Dalrymple and E. R. MacKow, “Roles for endothelial cells in dengue virus infection,” Advances in Virology, vol. 2012, Article ID 840654, 8 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. D. T. Trung and B. Wills, “Systemic vascular leakage associated with dengue infections—the clinical perspective,” Current Topics in Microbiology and Immunology, vol. 338, no. 1, pp. 57–66, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. C. F. Spiropoulou and A. Srikiatkhachorn, “The role of endothelial activation in dengue hemorrhagic fever and hantavirus pulmonary syndrome,” Virulence, vol. 4, no. 6, pp. 525–536, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Green and A. Rothman, “Immunopathological mechanisms in dengue and dengue hemorrhagic fever,” Current Opinion in Infectious Diseases, vol. 19, no. 5, pp. 429–436, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. WHO, Dengue Guidelines for Diagnosis, Treatment, Prevention and Control, World Health Organization, Geneva, Switzerland, 3rd edition, 2009.
  13. C. H. Roberts, J. Mongkolsapaya, and G. Screaton, “New opportunities for control of dengue virus,” Current Opinion in Infectious Diseases, vol. 26, no. 6, pp. 567–574, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. M. N. Krishnan and M. A. Garcia-Blanco, “Targeting host factors to treat West Nile and dengue viral infections,” Viruses, vol. 6, no. 2, pp. 683–708, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. J. L. Kyle, P. R. Beatty, and E. Harris, “Dengue virus infects macrophages and dendritic cells in a mouse model of infection,” Journal of Infectious Diseases, vol. 195, no. 12, pp. 1808–1817, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. S. B. Halstead, E. J. O'Rourke, and A. C. Allison, “Dengue viruses and mononuclear phagocytes. II. Identity of blood and tissue leukocytes supporting in vitro infection,” The Journal of Experimental Medicine, vol. 146, no. 1, pp. 218–229, 1977. View at Publisher · View at Google Scholar · View at Scopus
  17. M. A. Schmid, M. S. Diamond, and E. Harris, “Dendritic cells in dengue virus infection: targets of virus replication and mediators of immunity,” Frontiers in Immunology, vol. 5, article 647, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Lo Cicero, P. D. Stahl, and G. Raposo, “Extracellular vesicles shuffling intercellular messages: for good or for bad,” Current Opinion in Cell Biology, vol. 35, pp. 69–77, 2015. View at Publisher · View at Google Scholar
  19. J. M. Carr, H. Hocking, K. Bunting et al., “Supernatants from dengue virus type-2 infected macrophages induce permeability changes in endothelial cell monolayers,” Journal of Medical Virology, vol. 69, no. 4, pp. 521–528, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. Y.-C. Chen and S.-Y. Wang, “Activation of terminally differentiated human monocytes/macrophages by dengue virus: productive infection, hierarchical production of innate cytokines and chemokines, and the synergistic effect of lipopolysaccharide,” Journal of Virology, vol. 76, no. 19, pp. 9877–9887, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. Y.-C. Chen, S.-Y. Wang, and C.-C. King, “Bacterial lipopolysaccharide inhibits dengue virus infection of primary human monocytes/macrophages by blockade of virus entry via a CD14-dependent mechanism,” Journal of Virology, vol. 73, no. 4, pp. 2650–2657, 1999. View at Google Scholar · View at Scopus
  22. D.-M. Chang and M.-F. Shaio, “Production of interleukin-1 (IL-1) and IL-1 inhibitor by human monocytes exposed to dengue virus,” The Journal of Infectious Diseases, vol. 170, no. 4, pp. 811–817, 1994. View at Publisher · View at Google Scholar · View at Scopus
  23. I. Assunção-Miranda, F. A. Amaral, F. A. Bozza et al., “Contribution of macrophage migration inhibitory factor to the pathogenesis of dengue virus infection,” The FASEB Journal, vol. 24, no. 1, pp. 218–228, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. C. Chuang, H. R. Chen, and T. M. Yeh, “Pathogenic roles of macrophage migration inhibitory factor during dengue virus infection,” Mediators of Inflammation, vol. 2015, Article ID 547094, 7 pages, 2015. View at Publisher · View at Google Scholar
  25. L.-J. Ho, J.-J. Wang, M.-F. Shaio et al., “Infection of human dendritic cells by Dengue virus causes cell maturation and cytokine production,” The Journal of Immunology, vol. 166, no. 3, pp. 1499–1506, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. D. H. Libraty, S. Pichyangkul, C. Ajariyakhajorn, T. P. Endy, and F. A. Ennis, “Human dendritic cells are activated by dengue virus infection: enhancement by gamma interferon and implications for disease pathogenesis,” Journal of Virology, vol. 75, no. 8, pp. 3501–3508, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Luplerdlop, D. Missé, D. Bray et al., “Dengue-virus-infected dendritic cells trigger vascular leakage through metalloproteinase overproduction,” EMBO Reports, vol. 7, no. 11, pp. 1176–1181, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Anderson, S. Wang, C. Osiowy, and A. C. Issekutz, “Activation of endothelial cells via antibody-enhanced dengue virus infection of peripheral blood monocytes,” Journal of Virology, vol. 71, no. 6, pp. 4226–4232, 1997. View at Google Scholar · View at Scopus
  29. S. M. Bonner and M. A. O'Sullivan, “Endothelial cell monolayers as a model system to investigate dengue shock syndrome,” Journal of Virological Methods, vol. 71, no. 2, pp. 159–167, 1998. View at Publisher · View at Google Scholar · View at Scopus
  30. B. E. Dewi, T. Takasaki, and I. Kurane, “In vitro assessment of human endothelial cell permeability: effects of inflammatory cytokines and dengue virus infection,” Journal of Virological Methods, vol. 121, no. 2, pp. 171–180, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. D. Talavera, A. M. Castillo, M. C. Dominguez, A. E. Gutierrez, and I. Meza, “IL8 release, tight junction and cytoskeleton dynamic reorganization conducive to permeability increase are induced by dengue virus infection of microvascular endothelial monolayers,” Journal of General Virology, vol. 85, no. 7, pp. 1801–1813, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Liu, M. Woda, F. A. Ennis, and D. H. Libraty, “Dengue virus infection differentially regulates endothelial barrier function over time through type I interferon effects,” The Journal of Infectious Diseases, vol. 200, no. 2, pp. 191–201, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. J. E. Cardier, E. Mariño, E. Romano et al., “Proinflammatory factors present in sera from patients with acute dengue infection induce activation and apoptosis of human microvascular endothelial cells: possible role of TNF-alpha in endothelial cell damage in dengue,” Cytokine, vol. 30, no. 6, pp. 359–365, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Srikiatkhachorn, C. Ajariyakhajorn, T. P. Endy et al., “Virus-induced decline in soluble vascular endothelial growth receptor 2 is associated with plasma leakage in dengue hemorrhagic fever,” Journal of Virology, vol. 81, no. 4, pp. 1592–1600, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. J. E. Cardier, B. Rivas, E. Romano et al., “Evidence of vascular damage in dengue disease: demonstration of high levels of soluble cell adhesion molecules and circulating endothelial cells,” Endothelium, vol. 13, no. 5, pp. 335–340, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Lindner, J. Haier, Z. Wang, D. I. Watson, D. J. Hussey, and R. Hummel, “Circulating microRNAs: emerging biomarkers for diagnosis and prognosis in patients with gastrointestinal cancers,” Clinical Science, vol. 128, no. 1, pp. 1–15, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. D. G. Souza, C. T. Fagundes, L. P. Sousa et al., “Essential role of platelet-activating factor receptor in the pathogenesis of Dengue virus infection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 33, pp. 14138–14143, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Puerta-Guardo, A. Raya-Sandino, L. González-Mariscal et al., “The cytokine response of U937-derived macrophages infected through antibody-dependent enhancement of dengue virus disrupts cell apical-junction complexes and increases vascular permeability,” Journal of Virology, vol. 87, no. 13, pp. 7486–7501, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Y. Z. Li, K. McNicholas, T. Y. Yong et al., “BK virus encoded microRNAs are present in blood of renal transplant recipients with BK viral nephropathy,” American Journal of Transplantation, vol. 14, no. 5, pp. 1183–1190, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. K. J. Humphreys, R. A. McKinnon, and M. Z. Michael, “mir-18a inhibits CDC42 and plays a tumour suppressor role in colorectal cancer cells,” PLoS ONE, vol. 9, no. 11, Article ID e112288, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. E. L. de Azeredo, R. Q. Monteiro, and L. M. D.-O. Pinto, “Thrombocytopenia in dengue: interrelationship between virus and the imbalance between coagulation and fibrinolysis and inflammatory mediators,” Mediators of Inflammation, vol. 2015, Article ID 313842, 16 pages, 2015. View at Publisher · View at Google Scholar
  42. L. T. Hoang, D. J. Lynn, M. Henn et al., “The early whole-blood transcriptional signature of dengue virus and features associated with progression to dengue shock syndrome in Vietnamese children and young adults,” Journal of Virology, vol. 84, no. 24, pp. 12982–12994, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. Y.-H. Huang, H.-Y. Lei, H.-S. Liu et al., “Tissue plasminogen activator induced by dengue virus infection of human endothelial cells,” Journal of Medical Virology, vol. 70, no. 4, pp. 610–616, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. Y.-H. Huang, H.-Y. Lei, H.-S. Liu, Y.-S. Lin, C.-C. Liu, and T.-M. Yeh, “Dengue virus infects human endothelial cells and induces IL-6 and IL-8 production,” The American Journal of Tropical Medicine & Hygiene, vol. 63, no. 1-2, pp. 71–75, 2000. View at Google Scholar · View at Scopus
  45. D. Hober, L. Poli, B. Roblin et al., “Serum levels of tumor necrosis factor-alpha (TNF-alpha), interleukin-6 (IL-6), and interleukin-1 beta (IL-1 beta) in dengue-infected patients,” The American Journal of Tropical Medicine & Hygiene, vol. 48, no. 3, pp. 324–331, 1993. View at Google Scholar · View at Scopus
  46. L. Kittigul, W. Temprom, D. Sujirarat, and C. Kittigul, “Determination of tumor necrosis factor-alpha levels in dengue virus infected patients by sensitive biotin-streptavidin enzyme-linked immunosorbent assay,” Journal of Virological Methods, vol. 90, no. 1, pp. 51–57, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. F. A. Bozza, O. G. Cruz, S. M. O. Zagne et al., “Multiplex cytokine profile from dengue patients: MIP-1beta and IFN-gamma as predictive factors for severity,” BMC Infectious Diseases, vol. 8, article 86, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. A. S. Pacsa, R. Agarwal, E. A. Elbishbishi, U. C. Chaturvedi, R. Nagar, and A. S. Mustafa, “Role of interleukin-12 in patients with dengue hemorrhagic fever,” FEMS Immunology and Medical Microbiology, vol. 28, no. 2, pp. 151–155, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. M. T. Arévalo, P. J. Simpson-Haidaris, Z. Kou, J. J. Schlesinger, and X. Jin, “Primary human endothelial cells support direct but not antibody-dependent enhancement of dengue viral infection,” Journal of Medical Virology, vol. 81, no. 3, pp. 519–528, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Avirutnan, P. Malasit, B. Seliger, S. Bhakdi, and M. Husmann, “Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis,” Journal of Immunology, vol. 161, no. 11, pp. 6338–6346, 1998. View at Google Scholar · View at Scopus
  51. A. Basu, P. Jain, P. Sarkar et al., “Dengue virus infection of SK Hep1 cells: inhibition of in vitro angiogenesis and altered cytomorphology by expressed viral envelope glycoprotein,” FEMS Immunology and Medical Microbiology, vol. 62, no. 2, pp. 140–147, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Bunyaratvej, P. Butthep, S. Yoksan, and N. Bhamarapravati, “Dengue viruses induce cell proliferation and morphological changes of endothelial cells,” Southeast Asian Journal of Tropical Medicine & Public Health, vol. 28, supplement 3, pp. 32–37, 1997. View at Google Scholar · View at Scopus
  53. T. M. da Conceição, N. M. Rust, A. C. E. R. Berbel et al., “Essential role of RIG-I in the activation of endothelial cells by dengue virus,” Virology, vol. 435, no. 2, pp. 281–292, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Dalrymple and E. R. Mackow, “Productive dengue virus infection of human endothelial cells is directed by heparan sulfate-containing proteoglycan receptors,” Journal of Virology, vol. 85, no. 18, pp. 9478–9485, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. J. K. Calvert, K. J. Helbig, D. Dimasi et al., “Dengue virus infection of primary endothelial cells induces innate immune responses, changes in endothelial cells function and is restricted by interferon-stimulated responses,” Journal of Interferon & Cytokine Research, vol. 35, no. 8, pp. 654–665, 2015. View at Publisher · View at Google Scholar
  56. R. V. Warke, K. Xhaja, K. J. Martin et al., “Dengue virus induces novel changes in gene expression of human umbilical vein endothelial cells,” Journal of Virology, vol. 77, no. 21, pp. 11822–11832, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. C. N. Peyrefitte, B. Pastorino, G. E. Grau, J. Lou, H. Tolou, and P. Couissinier-Paris, “Dengue virus infection of human microvascular endothelial cells from different vascular beds promotes both common and specific functional changes,” Journal of Medical Virology, vol. 78, no. 2, pp. 229–242, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. T. F. Póvoa, A. M. B. Alves, C. A. B. Oliveira, G. J. Nuovo, V. L. A. Chagas, and M. V. Paes, “The pathology of severe dengue in multiple organs of human fatal cases: histopathology, ultrastructure and virus replication,” PLoS ONE, vol. 9, no. 4, Article ID e83386, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. S. J. Balsitis, J. Coloma, G. Castro et al., “Tropism of dengue virus in mice and humans defined by viral nonstructural protein 3-specific immunostaining,” American Journal of Tropical Medicine and Hygiene, vol. 80, no. 3, pp. 416–424, 2009. View at Google Scholar · View at Scopus
  60. K. Jessie, M. Y. Fong, S. Devi, S. K. Lam, and K. T. Wong, “Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization,” Journal of Infectious Diseases, vol. 189, no. 8, pp. 1411–1418, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. K. J. L. Liew and V. T. K. Chow, “Microarray and real-time RT-PCR analyses of a novel set of differentially expressed human genes in ECV304 endothelial-like cells infected with dengue virus type 2,” Journal of Virological Methods, vol. 131, no. 1, pp. 47–57, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. N. A. Dalrymple and E. R. Mackow, “Endothelial cells elicit immune-enhancing responses to dengue virus infection,” Journal of Virology, vol. 86, no. 12, pp. 6408–6415, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. Y.-T. Yen, H.-C. Chen, Y.-D. Lin, C.-C. Shieh, and B. A. Wu-Hsieh, “Enhancement by tumor necrosis factor alpha of dengue virus-induced endothelial cell production of reactive nitrogen and oxygen species is key to hemorrhage development,” Journal of Virology, vol. 82, no. 24, pp. 12312–12324, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. H.-C. Chen, F. M. Hofman, J. T. Kung, Y.-D. Lin, and B. A. Wu-Hsieh, “Both virus and tumor necrosis factor alpha are critical for endothelium damage in a mouse model of dengue virus-induced hemorrhage,” Journal of Virology, vol. 81, no. 11, pp. 5518–5526, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. R. M. Zellweger, T. R. Prestwood, and S. Shresta, “Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease,” Cell Host and Microbe, vol. 7, no. 2, pp. 128–139, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. J. R. Teijaro, K. B. Walsh, S. Cahalan et al., “Endothelial cells are central orchestrators of cytokine amplification during influenza virus infection,” Cell, vol. 146, no. 6, pp. 980–991, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. D. Safronetz, J. Prescott, F. Feldmann et al., “Pathophysiology of hantavirus pulmonary syndrome in rhesus macaques,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 19, pp. 7114–7119, 2014. View at Publisher · View at Google Scholar · View at Scopus
  68. S. M. Pitson, “Regulation of sphingosine kinase and sphingolipid signaling,” Trends in Biochemical Sciences, vol. 36, no. 2, pp. 97–107, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. X. Li, M. Stankovic, C. S. Bonder et al., “Basal and angiopoietin-1-mediated endothelial permeability is regulated by sphingosine kinase-1,” Blood, vol. 111, no. 7, pp. 3489–3497, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. W. Y. Sun, S. M. Pitson, and C. S. Bonder, “Tumor necrosis factor-induced neutrophil adhesion occurs via sphingosine kinase-1-dependent activation of endothelial α5β1 integrin,” The American Journal of Pathology, vol. 177, no. 1, pp. 436–446, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. J. R. Gamble, W. Y. Sun, X. Li et al., “Sphingosine kinase-1 associates with integrin αVβ3 to mediate endothelial cell survival,” American Journal of Pathology, vol. 175, no. 5, pp. 2217–2225, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. T. M. Leclercq and S. M. Pitson, “Cellular signalling by sphingosine kinase and sphingosine 1-phosphate,” IUBMB Life, vol. 58, no. 8, pp. 467–472, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. S. E. Alvarez, K. B. Harikumar, N. C. Hait et al., “Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2,” Nature, vol. 465, no. 7301, pp. 1084–1088, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. P. Xia, L. Wang, P. A. B. Moretti et al., “Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-α signaling,” Journal of Biological Chemistry, vol. 277, no. 10, pp. 7996–8003, 2002. View at Publisher · View at Google Scholar · View at Scopus
  75. H. Li and X. Lin, “Positive and negative signaling components involved in TNFα-induced NF-κB activation,” Cytokine, vol. 41, no. 1, pp. 1–8, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. M. MacEyka and S. Spiegel, “Sphingolipid metabolites in inflammatory disease,” Nature, vol. 510, no. 7503, pp. 58–67, 2014. View at Publisher · View at Google Scholar · View at Scopus
  77. C. A. Oskeritzian, “Mast cell plasticity and sphingosine-1-phosphate in immunity, inflammation and cancer,” Molecular Immunology, vol. 63, no. 1, pp. 104–112, 2015. View at Publisher · View at Google Scholar · View at Scopus
  78. S. Wati, S. M. Rawlinson, R. A. Ivanov et al., “Tumour necrosis factor alpha (TNF-α) stimulation of cells with established dengue virus type 2 infection induces cell death that is accompanied by a reduced ability of TNF-α to activate nuclear factor κb and reduced sphingosine kinase-1 activity,” Journal of General Virology, vol. 92, no. 4, pp. 807–818, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. J. M. Carr, T. Kua, J. N. Clarke et al., “Reduced sphingosine kinase 1 activity in dengue virus type-2 infected cells can be mediated by the 3′ untranslated region of dengue virus type-2 RNA,” Journal of General Virology, vol. 94, no. 11, pp. 2437–2448, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. V. Limaye, P. Xia, C. Hahn et al., “Chronic increases in sphingosine kinase-1 activity induce a pro-inflammatory, pro-angiogenic phenotype in endothelial cells,” Cellular and Molecular Biology Letters, vol. 14, no. 3, pp. 424–441, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. K. B. Harikumar, J. W. Yester, M. J. Surace et al., “K63-linked polyubiquitination of transcription factor IRF1 is essential for IL-1-induced production of chemokines CXCL10 and CCL5,” Nature Immunology, vol. 15, no. 3, pp. 231–238, 2014. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Shresta, K. L. Sharar, D. M. Prigozhin, P. R. Beatty, and E. Harris, “Murine model for dengue virus-induced lethal disease with increased vascular permeability,” Journal of Virology, vol. 80, no. 20, pp. 10208–10217, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. M. R. Pitman and S. M. Pitson, “Inhibitors of the sphingosine kinase pathway as potential therapeutics,” Current Cancer Drug Targets, vol. 10, no. 4, pp. 354–367, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Pyne, R. Bittman, and N. J. Pyne, “Sphingosine kinase inhibitors and cancer: seeking the golden sword of hercules,” Cancer Research, vol. 71, no. 21, pp. 6576–6582, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. T. S. Elton, H. Selemon, S. M. Elton, and N. L. Parinandi, “Regulation of the MIR155 host gene in physiological and pathological processes,” Gene, vol. 532, no. 1, pp. 1–12, 2013. View at Publisher · View at Google Scholar · View at Scopus
  86. B. Sehnert, H. Burkhardt, J. T. Wessels et al., “NF-κB inhibitor targeted to activated endothelium demonstrates a critical role of endothelial NF-κB in immune-mediated diseases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 41, pp. 16556–16561, 2013. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Maceyka, S. Milstien, and S. Spiegel, “Sphingosine-1-phosphate: the Swiss army knife of sphingolipid signaling,” Journal of Lipid Research, vol. 50, supplement, pp. S272–S276, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. S. Spiegel and S. Milstien, “The outs and the ins of sphingosine-1-phosphate in immunity,” Nature Reviews Immunology, vol. 11, no. 6, pp. 403–415, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Ospina-Bedoya, N. Campillo-Pedroza, J. P. Franco-Salazar, and J. C. Gallego-Gómez, “Computational identification of dengue virus MicroRNA-like structures and their cellular targets,” Bioinformatics and Biology Insights, vol. 8, pp. 169–176, 2014. View at Publisher · View at Google Scholar · View at Scopus
  90. D.-S. Im, “Pharmacological tools for lysophospholipid GPCRs: development of agonists and antagonists for LPA and S1P receptors,” Acta Pharmacologica Sinica, vol. 31, no. 9, pp. 1213–1222, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. K. P. Cusack and R. H. Stoffel, “S1P1 receptor agonists: assessment of selectivity and current clinical activity,” Current Opinion in Drug Discovery and Development, vol. 13, no. 4, pp. 481–488, 2010. View at Google Scholar · View at Scopus
  92. M. Bigaud, D. Guerini, A. Billich, F. Bassilana, and V. Brinkmann, “Second generation S1P pathway modulators: research strategies and clinical developments,” Biochimica et Biophysica Acta—Molecular and Cell Biology of Lipids, vol. 1841, no. 5, pp. 745–758, 2014. View at Publisher · View at Google Scholar · View at Scopus
  93. I. N. Gavrilovskaya, E. E. Gorbunova, N. A. Mackow, and E. R. Mackow, “Hantaviruses direct endothelial cell permeability by sensitizing cells to the vascular permeability factor VEGF, while angiopoietin 1 and sphingosine 1-phosphate inhibit hantavirus-directed permeability,” Journal of Virology, vol. 82, no. 12, pp. 5797–5806, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. V. Brinkmann, A. Billich, T. Baumruker et al., “Fingolimod (FTY720): discovery and development of an oral drug to treat multiple sclerosis,” Nature Reviews Drug Discovery, vol. 9, no. 11, pp. 883–897, 2010. View at Publisher · View at Google Scholar · View at Scopus
  95. H. Rosen, G. Sanna, and C. Alfonso, “Egress: a receptor-regulated step in lymphocyte trafficking,” Immunological Reviews, vol. 195, pp. 160–177, 2003. View at Publisher · View at Google Scholar · View at Scopus
  96. L. Wang, E. T. Chiang, J. T. Simmons, J. G. N. Garcia, and S. M. Dudek, “FTY720-induced human pulmonary endothelial barrier enhancement is mediated by c-Abl,” European Respiratory Journal, vol. 38, no. 1, pp. 78–88, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. R. C. Lee, R. L. Feinbaum, and V. Ambros, “The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14,” Cell, vol. 75, no. 5, pp. 843–854, 1993. View at Publisher · View at Google Scholar · View at Scopus
  98. D. P. Bartel, “MicroRNAs: genomics, biogenesis, mechanism, and function,” Cell, vol. 116, no. 2, pp. 281–297, 2004. View at Publisher · View at Google Scholar · View at Scopus
  99. R. C. Friedman, K. K.-H. Farh, C. B. Burge, and D. P. Bartel, “Most mammalian mRNAs are conserved targets of microRNAs,” Genome Research, vol. 19, no. 1, pp. 92–105, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. P. A. Tambyah, S. Chai, S. Sepramaniam, J. M. Ali, A. Armugam, and K. Jeyaseelan, “microRNA expression in blood of dengue patients,” Annals of Clinical Biochemistry, 2015. View at Publisher · View at Google Scholar
  101. H.-L. Jong, M. R. Mustafa, P. M. Vanhoutte, S. AbuBakar, and P.-F. Wong, “MicroRNA 299-3p modulates replicative senescence in endothelial cells,” Physiological Genomics, vol. 45, no. 7, pp. 256–267, 2013. View at Publisher · View at Google Scholar · View at Scopus
  102. Y. Qi, Y. Li, L. Zhang, and J. Huang, “MicroRNA expression profiling and bioinformatic analysis of dengue virus-infected peripheral blood mononuclear cells,” Molecular Medicine Reports, vol. 7, no. 3, pp. 791–798, 2013. View at Publisher · View at Google Scholar · View at Scopus
  103. M. Li, X. Y. He, Z. M. Zhang et al., “MicroRNA-1290 promotes esophageal squamous cell carcinoma cell proliferation and metastasis,” World Journal of Gastroenterology, vol. 21, no. 11, pp. 3245–3255, 2015. View at Google Scholar
  104. D. Karunakaran, A. B. Thrush, M. A. Nguyen et al., “Macrophage mitochondrial energy status regulates cholesterol efflux and is enhanced by anti-miR33 in atherosclerosis,” Circulation Research, vol. 117, no. 3, pp. 266–278, 2015. View at Publisher · View at Google Scholar
  105. G. Carvalheira, B. H. Nozima, and J. M. Cerutti, “MicroRNA-106b-mediated down-regulation of C1orf24 expression induces apoptosis and suppresses invasion of thyroid cancer,” Oncotarget, vol. 6, no. 29, pp. 28357–28370, 2015. View at Publisher · View at Google Scholar
  106. X. Zhu, Z. He, Y. Hu et al., “MicroRNA-30e* suppresses dengue virus replication by promoting NF-kappaB-dependent IFN production,” PLoS Neglected Tropical Diseases, vol. 8, no. 8, Article ID e3088, 2014. View at Publisher · View at Google Scholar
  107. P. K. Kakumani, S. S. Ponia, K. S. Rajgokul et al., “Role of RNA interference (RNAi) in dengue virus replication and identification of NS4B as an RNAi suppressor,” Journal of Virology, vol. 87, no. 16, pp. 8870–8883, 2013. View at Publisher · View at Google Scholar · View at Scopus
  108. H. P. Bogerd, R. L. Skalsky, E. M. Kennedy et al., “Replication of many human viruses is refractory to inhibition by endogenous cellular microRNAs,” Journal of Virology, vol. 88, no. 14, pp. 8065–8076, 2014. View at Publisher · View at Google Scholar · View at Scopus
  109. B. Qin, H. Yang, and B. Xiao, “Role of microRNAs in endothelial inflammation and senescence,” Molecular Biology Reports, vol. 39, no. 4, pp. 4509–4518, 2012. View at Publisher · View at Google Scholar · View at Scopus
  110. A. Chamorro-Jorganes, E. Araldi, and Y. Suárez, “MicroRNAs as pharmacological targets in endothelial cell function and dysfunction,” Pharmacological Research, vol. 75, pp. 15–27, 2013. View at Publisher · View at Google Scholar · View at Scopus
  111. J. L. Marques-Rocha, M. Samblas, F. I. Milagro, J. Bressan, J. A. Martinez, and A. Marti, “Noncoding RNAs, cytokines, and inflammation-related diseases,” The FASEB Journal, vol. 29, no. 9, pp. 3595–3611, 2015. View at Publisher · View at Google Scholar
  112. N. Wu, N. Gao, D. Fan, J. Wei, J. Zhang, and J. An, “miR-223 inhibits dengue virus replication by negatively regulating the microtubule-destabilizing protein STMN1 in EAhy926cells,” Microbes and Infection, vol. 16, no. 11, pp. 911–922, 2014. View at Publisher · View at Google Scholar · View at Scopus
  113. F. Taïbi, V. Metzinger-Le Meuth, Z. A. Massy, and L. Metzinger, “MiR-223: an inflammatory oncomiR enters the cardiovascular field,” Biochimica et Biophysica Acta, vol. 1842, no. 7, pp. 1001–1009, 2014. View at Publisher · View at Google Scholar · View at Scopus
  114. L. Shi, B. Fisslthaler, N. Zippel et al., “MicroRNA-223 antagonizes angiogenesis by targeting β1 integrin and preventing growth factor signaling in endothelial cells,” Circulation Research, vol. 113, no. 12, pp. 1320–1330, 2013. View at Publisher · View at Google Scholar · View at Scopus
  115. B. Laffont, A. Corduan, H. Plé et al., “Activated platelets can deliver mRNA regulatory Ago2•microRNA complexes to endothelial cells via microparticles,” Blood, vol. 122, no. 2, pp. 253–261, 2013. View at Publisher · View at Google Scholar
  116. Y. Saito, J. M. Friedman, Y. Chihara, G. Egger, J. C. Chuang, and G. Liang, “Epigenetic therapy upregulates the tumor suppressor microRNA-126 and its host gene EGFL7 in human cancer cells,” Biochemical and Biophysical Research Communications, vol. 379, no. 3, pp. 726–731, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. S. Wang, A. B. Aurora, B. A. Johnson et al., “The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis,” Developmental Cell, vol. 15, no. 2, pp. 261–271, 2008. View at Publisher · View at Google Scholar · View at Scopus
  118. J. E. Fish, M. M. Santoro, S. U. Morton et al., “miR-126 regulates angiogenic signaling and vascular integrity,” Developmental Cell, vol. 15, no. 2, pp. 272–284, 2008. View at Publisher · View at Google Scholar · View at Scopus
  119. T. A. Harris, M. Yamakuchi, M. Kondo, P. Oettgen, and C. J. Lowenstein, “Ets-1 and Ets-2 regulate the expression of microRNA-126 in endothelial cells,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, no. 10, pp. 1990–1997, 2010. View at Publisher · View at Google Scholar · View at Scopus
  120. K. Barton, N. Muthusamy, C. Fischer et al., “The Ets-1 transcription factor is required for the development of natural killer cells in mice,” Immunity, vol. 9, no. 4, pp. 555–563, 1998. View at Publisher · View at Google Scholar · View at Scopus
  121. H. Yamamoto, M. L. Flannery, S. Kupriyanov et al., “Defective trophoblast function in mice with a targeted mutation of Ets2,” Genes & Development, vol. 12, no. 9, pp. 1315–1326, 1998. View at Publisher · View at Google Scholar · View at Scopus
  122. T. A. Harris, M. Yamakuchi, M. Ferlito, J. T. Mendell, and C. J. Lowenstein, “MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 5, pp. 1516–1521, 2008. View at Publisher · View at Google Scholar · View at Scopus
  123. C. Johne, D. Matenia, X.-Y. Li, T. Timm, K. Balusamy, and E.-M. Mandelkow, “Spred1 and TESK1—two new interaction partners of the kinase MARKK/TAO1 that link the microtubule and actin cytoskeleton,” Molecular Biology of the Cell, vol. 19, no. 4, pp. 1391–1403, 2008. View at Publisher · View at Google Scholar · View at Scopus
  124. M. V. Suurna, S. L. Ashworth, M. Hosford et al., “Cofilin mediates ATP depletion-induced endothelial cell actin alterations,” American Journal of Physiology—Renal Physiology, vol. 290, no. 6, pp. F1398–F1407, 2006. View at Publisher · View at Google Scholar · View at Scopus
  125. J. Agudo, A. Ruzo, N. Tung et al., “The miR-126-VEGFR2 axis controls the innate response to pathogen-associated nucleic acids,” Nature Immunology, vol. 15, no. 1, pp. 54–62, 2014. View at Publisher · View at Google Scholar · View at Scopus
  126. R. M. O'Connell, K. D. Taganov, M. P. Boldin, G. Cheng, and D. Baltimore, “MicroRNA-155 is induced during the macrophage inflammatory response,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 5, pp. 1604–1609, 2007. View at Publisher · View at Google Scholar · View at Scopus
  127. H.-X. Sun, D.-Y. Zeng, R.-T. Li et al., “Essential role of microRNA-155 in regulating endothelium-dependent vasorelaxation by targeting endothelial nitric oxide synthase,” Hypertension, vol. 60, no. 6, pp. 1407–1414, 2012. View at Publisher · View at Google Scholar · View at Scopus
  128. N. Zhu, D. Zhang, S. Chen et al., “Endothelial enriched microRNAs regulate angiotensin II-induced endothelial inflammation and migration,” Atherosclerosis, vol. 215, no. 2, pp. 286–293, 2011. View at Publisher · View at Google Scholar · View at Scopus
  129. W. N. Durán, J. W. Breslin, and F. A. Sánchez, “The NO cascade, eNOS location, and microvascular permeability,” Cardiovascular Research, vol. 87, no. 2, pp. 254–261, 2010. View at Publisher · View at Google Scholar · View at Scopus
  130. Y. Altuvia, P. Landgraf, G. Lithwick et al., “Clustering and conservation patterns of human microRNAs,” Nucleic Acids Research, vol. 33, no. 8, pp. 2697–2706, 2005. View at Publisher · View at Google Scholar · View at Scopus
  131. M. Duan, H. Yao, G. Hu, X. Chen, A. K. Lund, and S. Buch, “HIV Tat induces expression of ICAM-1 in HUVECs: implications for miR-221/-222 in HIV-associated cardiomyopathy,” PLoS ONE, vol. 8, no. 3, Article ID e60170, 2013. View at Publisher · View at Google Scholar · View at Scopus
  132. C. F. Chen, J. Huang, H. Li et al., “MicroRNA-221 regulates endothelial nitric oxide production and inflammatory response by targeting adiponectin receptor 1,” Gene, vol. 565, no. 2, pp. 246–251, 2015. View at Publisher · View at Google Scholar
  133. Y. Zhan, C. Brown, E. Maynard et al., “Ets-1 is a critical regulator of Ang II-mediated vascular inflammation and remodeling,” The Journal of Clinical Investigation, vol. 115, no. 9, pp. 2508–2516, 2005. View at Publisher · View at Google Scholar · View at Scopus
  134. P. Oettgen, “Regulation of vascular inflammation and remodeling by ETS factors,” Circulation Research, vol. 99, no. 11, pp. 1159–1166, 2006. View at Publisher · View at Google Scholar · View at Scopus
  135. Y.-R. Lee, M.-T. Liu, H.-Y. Lei et al., “MCP1, a highly expressed chemokine in dengue haemorrhagic fever/dengue shock syndrome patients, may cause permeability change, possibly through reduced tight junctions of vascular endothelium cells,” Journal of General Virology, vol. 87, part 12, pp. 3623–3630, 2006. View at Publisher · View at Google Scholar · View at Scopus
  136. A. Ueda, Y. Ishigatsubo, T. Okubo, and T. Yoshimura, “Transcriptional regulation of the human monocyte chemoattractant protein-1 gene. Cooperation of two NF-κB sites and NF-κB/Rel subunit specificity,” The Journal of Biological Chemistry, vol. 272, no. 49, pp. 31092–31099, 1997. View at Publisher · View at Google Scholar · View at Scopus
  137. J. P. Hernández-Fonseca, A. Durán, N. Valero, and J. Mosquera, “Losartan and enalapril decrease viral absorption and interleukin 1 beta production by macrophages in an experimental dengue virus infection,” Archives of Virology, 2015. View at Publisher · View at Google Scholar
  138. R. C. S. Seet, A. W. L. Chow, A. M. L. Quek, Y.-H. Chan, and E. C. H. Lim, “Relationship between circulating vascular endothelial growth factor and its soluble receptors in adults with dengue virus infection: a case-control study,” International Journal of Infectious Diseases, vol. 13, no. 5, pp. e248–e253, 2009. View at Publisher · View at Google Scholar · View at Scopus
  139. T. Pepini, E. E. Gorbunova, I. N. Gavrilovskaya, J. E. Mackow, and E. R. Mackow, “Andes virus regulation of cellular microRNAs contributes to hantavirus-induced endothelial cell permeability,” Journal of Virology, vol. 84, no. 22, pp. 11929–11936, 2010. View at Publisher · View at Google Scholar · View at Scopus
  140. R. K. Jangra, M. Yi, and S. M. Lemon, “Regulation of hepatitis C virus translation and infectious virus production by the microRNA miR-122,” Journal of Virology, vol. 84, no. 13, pp. 6615–6625, 2010. View at Publisher · View at Google Scholar · View at Scopus
  141. Y. Endo-Takahashi, Y. Negishi, A. Nakamura et al., “Systemic delivery of miR-126 by miRNA-loaded Bubble liposomes for the treatment of hindlimb ischemia,” Scientific Reports, vol. 4, article 3883, 2014. View at Publisher · View at Google Scholar · View at Scopus
  142. J. Rohde, J. E. Weigand, B. Suess, and S. Dimmeler, “A universal aptamer chimera for the delivery of functional microRNA-126,” Nucleic Acid Therapeutics, vol. 25, no. 3, pp. 141–151, 2015. View at Publisher · View at Google Scholar
  143. M. E. Luck, S. A. Muljo, and C. B. Collins, “Prospects for therapeutic targeting of microRNAs in human immunological diseases,” The Journal of Immunology, vol. 194, no. 11, pp. 5047–5052, 2015. View at Google Scholar