DOI QR코드

DOI QR Code

Extravasating Neutrophil-derived Microparticles Preserve Vascular Barrier Function in Inflamed Tissue

  • Lim, Kihong (Department of Microbiology and Immunology, David H. Smith Center for Vaccine Biology and Immunology, University of Rochester) ;
  • Sumagin, Ronen (Epithelial Pathobiology and Mucosal Inflammation Research Unit, Department of Pathology and Laboratory Medicine, Emory University School of Medicine) ;
  • Hyun, Young-Min (Department of Microbiology and Immunology, David H. Smith Center for Vaccine Biology and Immunology, University of Rochester)
  • 투고 : 2013.05.14
  • 심사 : 2013.06.03
  • 발행 : 2013.06.30

초록

Emerging evidence suggests that gap formation and opening of the endothelial junctions during leukocyte extravasation is actively controlled to maintain the integrity of the vascular barrier. While the role for endothelial cells to this process has been well defined, it is not clear whether leukocytes are also actively contributing to endothelial barrier function. We have recently showed that extravasating leukocytes deposit microparticles on the subendothelium during the late stages of extravasation, which is LFA-1 dependent. Using multiphotonintravital microscopy (MP-IVM) of mouse cremaster muscle vessels in the current work, we show that microparticle formation and deposition maintains the integrity of the microvascular barrier during leukocyte extravasation. Inhibition of neutrophil-derived microparticle formation resulted in dramatically increased vascular leakage. These findings suggest that deposition of microparticles during neutrophil extravasation is essential for maintaining endothelial barrier function and may result in temporal difference between neutrophil extravasation and an increase in vascular leakage.

키워드

참고문헌

  1. Phillipson, M., B. Heit, P. Colarusso, L. Liu, C. M. Ballantyne, and P. Kubes. 2006. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J. Exp. Med. 203: 2569-2575. https://doi.org/10.1084/jem.20060925
  2. Shulman, Z., V. Shinder, E. Klein, V. Grabovsky, O. Yeger, E. Geron, A. Montresor, M. Bolomini-Vittori, S. W. Feigelson, T. Kirchhausen, C. Laudanna, G. Shakhar, and R. Alon. 2009. Lymphocyte crawling and transendothelial migration require chemokine triggering of high-affinity LFA-1 integrin. Immunity 30: 384-396. https://doi.org/10.1016/j.immuni.2008.12.020
  3. Sumagin, R., H. Prizant, E. Lomakina, R. E. Waugh, and I. H. Sarelius. 2010. LFA-1 and Mac-1 define characteristically different intralumenal crawling and emigration patterns for monocytes and neutrophils in situ. J. Immunol. 185: 7057-7066. https://doi.org/10.4049/jimmunol.1001638
  4. Auffray, C., D. Fogg, M. Garfa, G. Elain, O. Join-Lambert, S. Kayal, S. Sarnacki, A. CumG. Lauvau, and F. Geissmann. 2007. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317: 666-670. https://doi.org/10.1126/science.1142883
  5. Hyun, Y. M., R. Sumagin, P. P. Sarangi, E. Lomakina, M. G. Overstreet, C. M. Baker, D. J. Fowell, R. E. Waugh, I. H. Sarelius, and M. Kim. 2012. Uropod elongation is a common final step in leukocyte extravasation through inflamed vessels. J. Exp. Med. 209: 1349-1362. https://doi.org/10.1084/jem.20111426
  6. Sumagin, R., J. M. Kuebel, and I. H. Sarelius. 2011. Leukocyte rolling and adhesion both contribute to regulation of microvascular permeability to albumin via ligation of ICAM-1. Am. J. Physiol. Cell Physiol. 301: C804-813. https://doi.org/10.1152/ajpcell.00135.2011
  7. Boring, L., J. Gosling, S. W. Chensue, S. L. Kunkel, R. V. Farese Jr., H. E. Broxmeyer, and I. F. Charo. 1997. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J. Clin. Invest. 100: 2552-2561. https://doi.org/10.1172/JCI119798
  8. Dalli, J., L. V. Norling, D. Renshaw, D. Cooper, K. Y. Leung, and M. Perretti. 2008. Annexin 1 mediates the rapid anti-inflammatory effects of neutrophil-derived microparticles. Blood 112: 2512-2519. https://doi.org/10.1182/blood-2008-02-140533
  9. Daley, J. M., A. A. Thomay, M. D. Connolly, J. S. Reichner, and J. E. Albina. 2008. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 83: 64-70. https://doi.org/10.1189/jlb.0407247
  10. Soehnlein, O., A. Zernecke, E. E. Eriksson, A. G. Rothfuchs, C. T. Pham, H. Herwald, K. Bidzhekov, M. E. Rottenberg, C. Weber, and L. Lindbom. 2008. Neutrophil secretion products pave the way for inflammatory monocytes. Blood 112: 1461-1471. https://doi.org/10.1182/blood-2008-02-139634
  11. Woodfin, A., M. B. Voisin, M. Beyrau, B. Colom, D. Caille, F. M. Diapouli, G. B. Nash, T. Chavakis, S. M. Albelda, G. E. Rainger, P. Meda, B. A. Imhof, and S. Nourshargh. 2011. The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat. Immunol. 12: 761-769. https://doi.org/10.1038/ni.2062
  12. Kreisel, D., R. G. Nava, W. Li, B. H. Zinselmeyer, B. Wang, J. Lai, R. Pless, A. E. Gelman, A. S. Krupnick, and M. J. Miller. 2010. In vivo two-photon imaging reveals monocyte- dependent neutrophil extravasation during pulmonary inflammation. Proc. Natl. Acad. Sci. U. S. A. 107: 18073-18078. https://doi.org/10.1073/pnas.1008737107
  13. Van Rooijen, N. and A. Sanders. 1994. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods 174: 83-93 https://doi.org/10.1016/0022-1759(94)90012-4
  14. Geissmann, F., S. Jung, and D. R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19: 71-82. https://doi.org/10.1016/S1074-7613(03)00174-2
  15. Kim, J. V., S. S. Kang, M. L. Dustin, and D. B. McGavern. 2009. Myelomonocytic cell recruitment causes fatal CNS vascular injury during acute viral meningitis. Nature 457: 191-195 https://doi.org/10.1038/nature07591
  16. Bjork, J., P. Hedqvist, and K. E. Arfors. 1982. Increase in vascular permeability induced by leukotriene B4 and the role of polymorphonuclear leukocytes. Inflammation 6: 189-200. https://doi.org/10.1007/BF00916243
  17. Rosengren, S., K. Ley, and K. E. Arfors. 1989. Dextran sulfate prevents LTB4-induced permeability increase, but not neutrophil emigration, in the hamster cheek pouch. Microvasc. Res. 38: 243-254. https://doi.org/10.1016/0026-2862(89)90003-4
  18. Wedmore, C. V. and T. J. Williams. 1981. Control of vascular permeability by polymorphonuclear leukocytes in inflammation. Nature 289: 646-650. https://doi.org/10.1038/289646a0
  19. Herwald, H., H. Cramer, M. Morgelin, W. Russell, U. Sollenberg, A. Norrby-Teglund, H. Flodgaard, L. Lindbom, and L. Bjorck. 2004. M protein, a classical bacterial virulence determinant, forms complexes with fibrinogen that induce vascular leakage. Cell 116: 367-379. https://doi.org/10.1016/S0092-8674(04)00057-1
  20. Sekido, N., N. Mukaida, A. Harada, I. Nakanishi, Y. Watanabe, and K. Matsushima. 1993. Prevention of lung reperfusion injury in rabbits by a monoclonal antibody against interleukin-8. Nature 365: 654-657. https://doi.org/10.1038/365654a0
  21. Petri, B., J. Kaur, E. M. Long, H. Li, S. A. Parsons, S. Butz, M. Phillipson, D. Vestweber, K. D. Patel, S. M. Robbins, and P. Kubes. 2011. Endothelial LSP1 is involved in endothelial dome formation, minimizing vascular permeability changes during neutrophil transmigration in vivo. Blood 117: 942-952. https://doi.org/10.1182/blood-2010-02-270561
  22. Maus, U., K. von Grote, W. A. Kuziel, M. Mack, E. J. Miller, J. Cihak, M. Stangassinger, R. Maus, D. Schlondorff, W. Seeger, and J. Lohmeyer. 2002. The role of CC chemokine receptor 2 in alveolar monocyte and neutrophil immigration in intact mice. Am. J. Respir. Crit. Care Med. 166: 268-273. https://doi.org/10.1164/rccm.2112012

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