Neutrophil migration under normal and sepsis conditions

Cardiovascular and Hematological Disorders - Drug Targets

Volumn 15, Issue 1, 2015, Pages 19-28

  Lerman, Yelena V ^a   Kim, Minsoo ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Cell adhesion; Cell migration; Chemokine; Cytokine; Endothelial cell; Neutrophil; Sepsis

Indexed keywords

G PROTEIN COUPLED RECEPTOR; INTEGRIN; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL ADHESION; CELL MIGRATION; DIAPEDESIS; EXTRAVASATION; GRANULOPOIESIS; HUMAN; IMMUNE RESPONSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; SEPSIS; SIGNAL TRANSDUCTION; VIRUS RELEASE; ANIMAL; CELL MOTION; COMPLICATION; METABOLISM; MULTIPLE ORGAN FAILURE; PATHOPHYSIOLOGY; PHYSIOLOGY; SEVERITY OF ILLNESS INDEX; SURVIVAL;

ANIMALS; CELL MOVEMENT; HUMANS; MULTIPLE ORGAN FAILURE; NEUTROPHILS; REACTIVE OXYGEN SPECIES; SEPSIS; SEVERITY OF ILLNESS INDEX; SURVIVAL;

EID: 84953344651     PISSN: 1871529X     EISSN: None     Source Type: Journal    
DOI: 10.2174/1871529X15666150108113236     Document Type: Article

References (128)

1. Rittirsch, D.; Flierl, M.A.; Nadeau, B.A.; Day, D.E.; Huber-Lang, M.; Mackay, C.R.; Zetoune, F.S.; Gerard, N.P.; Cianflone, K.; Kohl, J.; Gerard, C.; Sarma, J.V.; Ward, P.A. Functional roles for C5a receptors in sepsis. Nat. Med., 2008, 14, 551-557.
2. Angus, D.C.; Linde-Zwirble, W.T.; Lidicker, J.; Clermont, G.; Carcillo, J.; Pinsky, M.R. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med., 2001, 29, 1303-1310.
3. Nathan, C. Neutrophils and immunity: challenges and opportunities. Nat Rev. Immunol., 2006, 6, 173-182.
4. Brown, K.A.; Brain, S.D.; Pearson, J.D.; Edgeworth, J.D.; Lewis, S.M.; Treacher, D.F. Neutrophils in development of multiple organ failure in sepsis. Lancet, 2006, 368, 157-169.
5. Cartwright, G.E.; Athens, J.W.; Wintrobe, M.M. The Kinetics of Granulopoiesis in Normal Man. Blood, 1964, 24, 780-803.
6. Demetri, G.D.; Griffin, J.D. Granulocyte colony-stimulating factor and its receptor. Blood, 1991, 78, 2791-2808.
7. Summers, C.; Rankin, S.M.; Condliffe, A.M.; Singh, N.; Peters, A. M.; Chilvers, E.R. Neutrophil kinetics in health and disease. Trends Immunol., 2010, 31, 318-324.
8. Friedman, A.D. Transcriptional control of granulocyte and monocyte development. Oncogene, 2007, 26, 6816-6828.
9. Kondo, M.; Wagers, A.J.; Manz, M.G.; Prohaska, S.S.; Scherer, D. C.; Beilhack, G.F.; Shizuru, J.A.; Weissman, I.L. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annual Rev. Immunol., 2003, 21, 759-806.
10. Iwasaki, H.; Akashi, K. Myeloid lineage commitment from the hematopoietic stem cell. Immunity, 2007, 26, 726-740.
11. Theilgaard-Monch, K.; Jacobsen, L.C.; Borup, R.; Rasmussen, T.; Bjerregaard, M.D.; Nielsen, F.C.; Cowland, J.B.; Borregaard, N. The transcriptional program of terminal granulocytic differentiation. Blood, 2005, 105, 1785-1796.
12. Fiedler, K.; Brunner, C. The role of transcription factors in the guidance of granulopoiesis. Am. J. Blood Res., 2012, 2, 57-65.
13. Richards, M.K.; Liu, F.; Iwasaki, H.; Akashi, K.; Link, D.C. Pivotal role of granulocyte colony-stimulating factor in the development of progenitors in the common myeloid pathway. Blood, 2003, 102, 3562-3568.
14. Lord, B.I.; Bronchud, M.H.; Owens, S.; Chang, J.; Howell, A.; Souza, L.; Dexter, T.M. The kinetics of human granulopoiesis following treatment with granulocyte colony-stimulating factor in vivo. Proc. Natl. Acad. Sci. USA, 1989, 86, 9499-9503.
15. Furze, R.C.; Rankin, S.M. Neutrophil mobilization and clearance in the bone marrow. Immunology, 2008, 125, 281-288.
16. Lieschke, G.J.; Grail, D.; Hodgson, G.; Metcalf, D.; Stanley, E.; Cheers, C.; Fowler, K.J.; Basu, S.; Zhan, Y.F.; Dunn, A.R. Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood, 1994, 84, 1737-1746.
17. Liu, F.; Wu, H.Y.; Wesselschmidt, R.; Kornaga, T.; Link, D.C. Impaired production and increased apoptosis of neutrophils in granulocyte colony-stimulating factor receptor-deficient mice. Immunity, 1996, 5, 491-501.
18. Sinha, S.; Zhu, Q.S.; Romero, G.; Corey, S.J. Deletional mutation of the external domain of the human granulocyte colonystimulating factor receptor in a patient with severe chronic neutropenia refractory to granulocyte colony-stimulating factor. J. Pediatr. Hematol. Oncol., 2003, 25, 791-796.
19. Druhan, L.J.; Ai, J.; Massullo, P.; Kindwall-Keller, T.; Ranalli, M. A.; Avalos, B.R. Novel mechanism of G-CSF refractoriness in patients with severe congenital neutropenia. Blood, 2005, 105, 584-591.
20. Liu, F.; Poursine-Laurent, J.; Wu, H.Y.; Link, D.C. Interleukin-6 and the granulocyte colony-stimulating factor receptor are major independent regulators of granulopoiesis in vivo but are not required for lineage commitment or terminal differentiation. Blood, 1997, 90, 2583-2590.
21. Seymour, J.F.; Lieschke, G.J.; Grail, D.; Quilici, C.; Hodgson, G.; Dunn, A.R. Mice lacking both granulocyte colony-stimulating factor (CSF) and granulocyte-macrophage CSF have impaired reproductive capacity, perturbed neonatal granulopoiesis, lung disease, amyloidosis, and reduced long-term survival. Blood, 1997, 90, 3037-3049.
22. Molineux, G.; Migdalska, A.; Szmitkowski, M.; Zsebo, K.; Dexter, T. M. The effects on hematopoiesis of recombinant stem cell factor (ligand for c-kit) administered in vivo to mice either alone or in combination with granulocyte colony-stimulating factor. Blood, 1991, 78, 961-966.
23. Stanley, E.; Lieschke, G.J.; Grail, D.; Metcalf, D.; Hodgson, G.; Gall, J.A.; Maher, D.W.; Cebon, J.; Sinickas, V.; Dunn, A.R. Granulocyte/macrophage colony-stimulating factor-deficient mice show no major perturbation of hematopoiesis but develop a characteristic pulmonary pathology. Proc. Natl. Acad. Sci. USA, 1994, 91, 5592-5596.
24. Kopf, M.; Baumann, H.; Freer, G.; Freudenberg, M.; Lamers, M.; Kishimoto, T.; Zinkernagel, R.; Bluethmann, H.; Kohler, G. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature, 1994, 368, 339-342.
25. Nishinakamura, R.; Miyajima, A.; Mee, P.J.; Tybulewicz, V.L.; Murray, R. Hematopoiesis in mice lacking the entire granulocytemacrophage colony-stimulating factor/interleukin-3/interleukin-5 functions. Blood, 1996, 88, 2458-2464.
26. Walker, F.; Zhang, H.H.; Matthews, V.; Weinstock, J.; Nice, E.C.; Ernst, M.; Rose-John, S.; Burgess, A. W. IL6/sIL6R complex contributes to emergency granulopoietic responses in G-CSF-and GM-CSF-deficient mice. Blood, 2008, 111, 3978-3985.
27. Kaushansky, K. Lineage-specific hematopoietic growth factors. N. Engl. J. Med., 2006, 354, 2034-2045.
28. Semerad, C.L.; Liu, F.; Gregory, A.D.; Stumpf, K.; Link, D.C. GCSF is an essential regulator of neutrophil trafficking from the bone marrow to the blood. Immunity, 2002, 17, 413-423.
29. Burdon, P.C.; Martin, C.; Rankin, S.M. Migration across the sinusoidal endothelium regulates neutrophil mobilization in response to ELR + CXC chemokines. Br. J. Haematol., 2008, 142, 100-108.
30. Eash, K.J.; Greenbaum, A.M.; Gopalan, P.K.; Link, D.C. CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J. Clin. Invest., 2010, 120, 2423-2431.
31. Eash, K.J.; Means, J.M.; White, D.W.; Link, D.C. CXCR4 is a key regulator of neutrophil release from the bone marrow under basal and stress granulopoiesis conditions. Blood, 2009, 113, 4711-4719.
32. Day, R.B.; Link, D.C. Regulation of neutrophil trafficking from the bone marrow. Cell. Mol. Life Sci., 2012, 69, 1415-1423.
33. Martin, C.; Burdon, P.C.; Bridger, G.; Gutierrez-Ramos, J.C.; Williams, T.J.; Rankin, S.M. Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity, 2003, 19, 583-593.
34. Hernandez, P.A.; Gorlin, R.J.; Lukens, J.N.; Taniuchi, S.; Bohinjec, J.; Francois, F.; Klotman, M.E.; Diaz, G.A. Mutations in the chemokine receptor gene CXCR4 are associated with WHIM syndrome, a combined immunodeficiency disease. Nat. Genet., 2003, 34, 70-74.
35. Diaz, G.A.; Gulino, A.V. WHIM syndrome: a defect in CXCR4 signaling. Curr. Allergy Asthma Rep., 2005, 5, 350-355.
36. Devine, S.M.; Vij, R.; Rettig, M.; Todt, L.; McGlauchlen, K.; Fisher, N.; Devine, H.; Link, D.C.; Calandra, G.; Bridger, G.; Westervelt, P.; Dipersio, J.F. Rapid mobilization of functional donor hematopoietic cells without G-CSF using AMD3100, an antagonist of the CXCR4/SDF-1 interaction. Blood, 2008, 112, 990-998.
37. Iyer, C.V.; Evans, R. J.; Lou, Q.; Lin, D.; Wang, J.; Kohn, W.; Yan, L. Z.; Pulley, S.; Peng, S.B. Rapid and recurrent neutrophil mobilization regulated by T134, a CXCR4 peptide antagonist. Exp. Hematol., 2008, 36, 1098-1109.
38. Pelus, L.M.; Bian, H.; Fukuda, S.; Wong, D.; Merzouk, A.; Salari, H. The CXCR4 agonist peptide, CTCE-0021, rapidly mobilizes polymorphonuclear neutrophils and hematopoietic progenitor cells into peripheral blood and synergizes with granulocyte colonystimulating factor. Exp. Hematol., 2005, 33, 295-307.
39. Link, D.C. Neutrophil homeostasis: a new role for stromal cellderived factor-1. Immunol. Res., 2005, 32, 169-178.
40. Suratt, B.T.; Petty, J.M.; Young, S.K.; Malcolm, K.C.; Lieber, J.G.; Nick, J.A.; Gonzalo, J.A.; Henson, P.M.; Worthen, G.S. Role of the CXCR4/SDF-1 chemokine axis in circulating neutrophil homeostasis. Blood, 2004, 104, 565-571.
41. Burdon, P.C.; Martin, C.; Rankin, S.M. The CXC chemokine MIP-2 stimulates neutrophil mobilization from the rat bone marrow in a CD49d-dependent manner. Blood, 2005, 105, 2543-2548.
42. Forlow, S.B.; Schurr, J.R.; Kolls, J.K.; Bagby, G.J.; Schwarzenberger, P.O.; Ley, K. Increased granulopoiesis through interleukin-17 and granulocyte colony-stimulating factor in leukocyte adhesion molecule-deficient mice. Blood, 2001, 98, 3309-3314.
43. Sarangi, P.P.; Hyun, Y.M.; Lerman, Y.V.; Pietropaoli, A.P.; Kim, M. Role of beta1 integrin in tissue homing of neutrophils during sepsis. Shock, 2012, 38, 281-287.
44. Jacobsen, K.; Kravitz, J.; Kincade, P.W.; Osmond, D.G. Adhesion receptors on bone marrow stromal cells: in vivo expression of vascular cell adhesion molecule-1 by reticular cells and sinusoidal endothelium in normal and gamma-irradiated mice. Blood, 1996, 87, 73-82.
45. Ulyanova, T.; Priestley, G.V.; Banerjee, E.R.; Papayannopoulou, T. Unique and redundant roles of alpha4 and beta2 integrins in kinetics of recruitment of lymphoid vs myeloid cell subsets to the inflamed peritoneum revealed by studies of genetically deficient mice. Exp. Hematol., 2007, 35, 1256-1265.
46. Diamond, M.S.; Staunton, D.E.; Marlin, S.D.; Springer, T.A. Binding of the integrin Mac-1 (CD11b/CD18) to the third Ig-like domain of ICAM-1 (CD54) and its regulation by glycosylation. Cell 1991, 65, 961-971.
47. Rothlein, R.; Dustin, M.L.; Marlin, S.D.; Springer, T.A. A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1. J. Immunol., 1986, 137, 1270-1274.
48. Springer, T.A. Adhesion receptors of the immune system. Nature, 1990, 346, 425-433.
49. Phillipson, M.; Heit, B.; Colarusso, P.; Liu, L.; Ballantyne, C.M.; Kubes, P. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J. Exp. Med., 2006, 203, 2569-2575.
50. Shulman, Z.; Shinder, V.; Klein, E.; Grabovsky, V.; Yeger, O.; Geron, E.; Montresor, A.; Bolomini-Vittori, M.; Feigelson, S.W.; Kirchhausen, T.; Laudanna, C.; Shakhar, G.; Alon, R. Lymphocyte crawling and transendothelial migration require chemokine triggering of high-affinity LFA-1 integrin. Immunity, 2009, 30, 384-396.
51. Auffray, C.; Fogg, D.; Garfa, M.; Elain, G.; Join-Lambert, O.; Kayal, S.; Sarnacki, S.; Cumano, A.; Lauvau, G.; Geissmann, F. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science, 2007, 317, 666-670.
52. Sorokin, L. The impact of the extracellular matrix on inflammation. Nat Rev. Immunol., 2010, 10, 712-723.
53. Wang, S.; Voisin, M.B.; Larbi, K.Y.; Dangerfield, J.; Scheiermann, C.; Tran, M.; Maxwell, P.H.; Sorokin, L.; Nourshargh, S. Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. J. Exp. Med., 2006, 203, 1519-1532.
54. Maus, U.; Huwe, J.; Ermert, L.; Ermert, M.; Seeger, W.; Lohmeyer, J. Molecular pathways of monocyte emigration into the alveolar air space of intact mice. Am. J. Respir. Crit. Care Med., 2002, 165, 95-100.
55. Smith, C.W.; Rothlein, R.; Hughes, B.J.; Mariscalco, M.M.; Rudloff, H.E.; Schmalstieg, F.C.; Anderson, D.C. Recognition of an endothelial determinant for CD 18-dependent human neutrophil adherence and transendothelial migration. J. Clin. Invest., 1988, 82, 1746-1756.
56. Woodfin, A.; Voisin, M.B.; Imhof, B.A.; Dejana, E.; Engelhardt, B.; Nourshargh, S. Endothelial cell activation leads to neutrophil transmigration as supported by the sequential roles of ICAM-2, JAM-A, and PECAM-1. Blood, 2009, 113, 6246-6257.
57. Vestweber, D. Adhesion and signaling molecules controlling the transmigration of leukocytes through endothelium. Immunol. Rev., 2007, 218, 178-196.
58. Carman, C.V.; Springer, T.A. Trans-cellular migration: cell-cell contacts get intimate. Curr. Opin. Cell Biol., 2008, 20, 533-540.
59. Burns, A.R.; Walker, D.C.; Brown, E.S.; Thurmon, L.T.; Bowden, R.A.; Keese, C.R.; Simon, S.I.; Entman, M.L.; Smith, C.W. Neutrophil transendothelial migration is independent of tight junctions and occurs preferentially at tricellular corners. J. Immunol., 1997, 159, 2893-2903.
60. Sumagin, R.; Sarelius, I.H. Intercellular adhesion molecule-1 enrichment near tricellular endothelial junctions is preferentially associated with leukocyte transmigration and signals for reorganization of these junctions to accommodate leukocyte passage. J. Immunol., 2010, 184, 5242-5252.
61. Mamdouh, Z.; Chen, X.; Pierini, L.M.; Maxfield, F.R.; Muller, W. A. Targeted recycling of PECAM from endothelial surfaceconnected compartments during diapedesis. Nature, 2003, 421, 748-753.
62. Shaw, S.K.; Bamba, P.S.; Perkins, B.N.; Luscinskas, F.W. Realtime imaging of vascular endothelial-cadherin during leukocyte transmigration across endothelium. J. Immunol., 2001, 167, 2323-2330.
63. Wegmann, F.; Petri, B.; Khandoga, A.G.; Moser, C.; Khandoga, A.; Volkery, S.; Li, H.; Nasdala, I.; Brandau, O.; Fassler, R.; Butz, S.; Krombach, F.; Vestweber, D. ESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability. J. Exp. Med., 2006, 203, 1671-1677.
64. Carman, C.V.; Springer, T.A. A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J. Cell. Biol., 2004, 167, 377-388.
65. Williams, S.L.; Milne, I.R.; Bagley, C.J.; Gamble, J.R.; Vadas, M. A.; Pitson, S.M.; Khew-Goodall, Y. A proinflammatory role for proteolytically cleaved annexin A1 in neutrophil transendothelial migration. J. Immunol., 2010, 185, 3057-3063.
66. Millan, J.; Hewlett, L.; Glyn, M.; Toomre, D.; Clark, P.; Ridley, A. J. Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola-and F-actin-rich domains. Nat. Cell Biol., 2006, 8, 113-123.
67. Phillipson, M.; Kaur, J.; Colarusso, P.; Ballantyne, C. M.; Kubes, P. Endothelial domes encapsulate adherent neutrophils and minimize increases in vascular permeability in paracellular and transcellular emigration. PLoS One, 2008, 3, e1649.
68. van Buul, J.D.; Allingham, M.J.; Samson, T.; Meller, J.; Boulter, E.; Garcia-Mata, R.; Burridge, K. RhoG regulates endothelial apical cup assembly downstream from ICAM1 engagement and is involved in leukocyte trans-endothelial migration. J. Cell Biol., 2007, 178, 1279-1293.
69. Feng, D.; Nagy, J.A.; Pyne, K.; Dvorak, H.F.; Dvorak, A.M. Neutrophils emigrate from venules by a transendothelial cell pathway in response to FMLP. J. Exp. Med., 1998, 187, 903-915.
70. Hyun, Y.M.; Sumagin, R.; Sarangi, P.P.; Lomakina, E.; Overstreet, M. G.; Baker, C.M.; Fowell, D.J.; Waugh, R.E.; Sarelius, I.H.; Kim, M. Uropod elongation is a common final step in leukocyte extravasation through inflamed vessels. J. Exp. Med., 2012, 209, 1349-1362.
71. Evans, B.J.; McDowall, A.; Taylor, P.C.; Hogg, N.; Haskard, D.O.; Landis, R.C. Shedding of lymphocyte function-associated antigen-1 (LFA-1) in a human inflammatory response. Blood, 2006, 107, 3593-3599.
72. Vaisar, T.; Kassim, S.Y.; Gomez, I.G.; Green, P.S.; Hargarten, S.; Gough, P.J.; Parks, W.C.; Wilson, C.L.; Raines, E.W.; Heinecke, J. W. MMP-9 sheds the beta2 integrin subunit (CD18) from macrophages. Mol. Cell. Proteomics, 2009, 8, 1044-1060.
73. Morin, N.A.; Oakes, P.W.; Hyun, Y.M.; Lee, D.; Chin, Y.E.; King, M.R.; Springer, T.A.; Shimaoka, M.; Tang, J.X.; Reichner, J.S.; Kim, M. Nonmuscle myosin heavy chain IIA mediates integrin LFA-1 de-adhesion during T lymphocyte migration. J. Exp. Med. 2008, 205, 195-205.
74. Ley, K.; Laudanna, C.; Cybulsky, M.I.; Nourshargh, S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev. Immunol., 2007, 7, 678-689.
75. Voisin, M.B.; Woodfin, A.; Nourshargh, S. Monocytes and neutrophils exhibit both distinct and common mechanisms in penetrating the vascular basement membrane in vivo. Arterioscler. Thromb. Vasc. Biol., 2009, 29, 1193-1199.
76. Voisin, M.B.; Probstl, D.; Nourshargh, S. Venular basement membranes ubiquitously express matrix protein low-expression regions: characterization in multiple tissues and remodeling during inflammation. Am. J. Pathol., 2010, 176, 482-495.
77. Young, R.E.; Thompson, R.D.; Larbi, K.Y.; La, M.; Roberts, C.E.; Shapiro, S.D.; Perretti, M.; Nourshargh, S. Neutrophil elastase (NE)-deficient mice demonstrate a nonredundant role for NE in neutrophil migration, generation of proinflammatory mediators, and phagocytosis in response to zymosan particles in vivo. J. Immunol., 2004, 172, 4493-4502.
78. Wang, S.; Dangerfield, J.P.; Young, R.E.; Nourshargh, S. PECAM-1, alpha6 integrins and neutrophil elastase cooperate in mediating neutrophil transmigration. J. Cell Sci., 2005, 118, 2067-2076.
79. Young, R.E.; Voisin, M.B.; Wang, S.; Dangerfield, J.; Nourshargh, S. Role of neutrophil elastase in LTB4-induced neutrophil transmigration in vivo assessed with a specific inhibitor and neutrophil elastase deficient mice. Br. J. Pharmacol., 2007, 151, 628-637.
80. Tkalcevic, J.; Novelli, M.; Phylactides, M.; Iredale, J.P.; Segal, A. W.; Roes, J. Impaired immunity and enhanced resistance to endotoxin in the absence of neutrophil elastase and cathepsin G. Immunity, 2000, 12, 201-210.
81. Hirche, T.O.; Atkinson, J.J.; Bahr, S.; Belaaouaj, A. Deficiency in neutrophil elastase does not impair neutrophil recruitment to inflamed sites. Am. J. Respir. Cell Mol. Biol., 2004, 30, 576-584.
82. Kubes, P.; Niu, X.F.; Smith, C.W.; Kehrli, M.E., Jr.; Reinhardt, P. H.; Woodman, R.C. A novel beta 1-dependent adhesion pathway on neutrophils: a mechanism invoked by dihydrocytochalasin B or endothelial transmigration. FASEB J., 1995, 9, 1103-1111.
83. Roussel, E.; Gingras, M.C. Transendothelial migration induces rapid expression on neutrophils of granule-release VLA6 used for tissue infiltration. J. Leukoc. Biol., 1997, 62, 356-362.
84. Werr, J.; Johansson, J.; Eriksson, E.E.; Hedqvist, P.; Ruoslahti, E.; Lindbom, L. Integrin alpha(2)beta(1) (VLA-2) is a principal receptor used by neutrophils for locomotion in extravascular tissue. Blood, 2000, 95, 1804-1809.
85. Werr, J.; Xie, X.; Hedqvist, P.; Ruoslahti, E.; Lindbom, L. Beta1 integrins are critically involved in neutrophil locomotion in extravascular tissue In vivo. J. Exp. Med., 1998, 187, 2091-2096.
86. Delano, M.J.; Kelly-Scumpia, K.M.; Thayer, T.C.; Winfield, R.D.; Scumpia, P.O.; Cuenca, A.G.; Harrington, P.B.; O’Malley, K.A.; Warner, E.; Gabrilovich, S.; Mathews, C.E.; Laface, D.; Heyworth, P.G.; Ramphal, R.; Strieter, R.M.; Moldawer, L.L.; Efron, P.A. Neutrophil mobilization from the bone marrow during polymicrobial sepsis is dependent on CXCL12 signaling. J. Immunol., 2011, 187, 911-918.
87. Christopher, M.J.; Link, D.C. Regulation of neutrophil homeostasis. Curr. Opin. Hematol., 2007, 14, 3-8.
88. Drost, E.M.; Kassabian, G.; Meiselman, H.J.; Gelmont, D.; Fisher, T.C. Increased rigidity and priming of polymorphonuclear leukocytes in sepsis. Am. J. Respir. Crit. Care Med., 1999, 159, 1696-1702.
89. Skoutelis, A.T.; Kaleridis, V.; Athanassiou, G.M.; Kokkinis, K.I.; Missirlis, Y.F.; Bassaris, H.P. Neutrophil deformability in patients with sepsis, septic shock, and adult respiratory distress syndrome. Crit. Care Med., 2000, 28, 2355-2359.
90. Saito, H.; Lai, J.; Rogers, R.; Doerschuk, C.M. Mechanical properties of rat bone marrow and circulating neutrophils and their responses to inflammatory mediators. Blood, 2002, 99, 2207-2213.
91. Reddy, R.C.; Narala, V.R.; Keshamouni, V.G.; Milam, J.E.; Newstead, M.W.; Standiford, T.J. Sepsis-induced inhibition of neutrophil chemotaxis is mediated by activation of peroxisome proliferator-activated receptor-{gamma}. Blood, 2008, 112, 4250-4258.
92. Zeuke, S.; Ulmer, A.J.; Kusumoto, S.; Katus, H.A.; Heine, H. TLR4-mediated inflammatory activation of human coronary artery endothelial cells by LPS. Cardiovasc. Res., 2002, 56, 126-134.
93. Sawa, Y.; Ueki, T.; Hata, M.; Iwasawa, K.; Tsuruga, E.; Kojima, H.; Ishikawa, H.; Yoshida, S. LPS-induced IL-6, IL-8, VCAM-1, and ICAM-1 expression in human lymphatic endothelium. J. Histochem. Cytochem., 2008, 56, 97-109.
94. Laudes, I.J.; Guo, R.F.; Riedemann, N.C.; Speyer, C.; Craig, R.; Sarma, J.V.; Ward, P.A. Disturbed homeostasis of lung intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 during sepsis. Am. J. Pathol., 2004, 164, 1435-1445.
95. Wu, R.Q.; Xu, Y.X.; Song, X.H.; Chen, L.J.; Meng, X.J. Adhesion molecule and proinflammatory cytokine gene expression in hepatic sinusoidal endothelial cells following cecal ligation and puncture. World J. Gastroenterol., 2001, 7, 128-130.
96. Ogawa, H.; Rafiee, P.; Heidemann, J.; Fisher, P.J.; Johnson, N.A.; Otterson, M.F.; Kalyanaraman, B.; Pritchard, K.A., Jr.; Binion, D. G. Mechanisms of endotoxin tolerance in human intestinal microvascular endothelial cells. J. Immunol., 2003, 170, 5956-5964.
97. van Den Engel, N.K.; Heidenthal, E.; Vinke, A.; Kolb, H.; Martin, S. Circulating forms of intercellular adhesion molecule (ICAM)-1 in mice lacking membranous ICAM-1. Blood, 2000, 95, 1350-1355.
98. Gearing, A.J.; Newman, W. Circulating adhesion molecules in disease. Immunol. Today, 1993, 14, 506-512.
99. Xu, H.; Gonzalo, J.A.; St Pierre, Y.; Williams, I.R.; Kupper, T.S.; Cotran, R.S.; Springer, T.A.; Gutierrez-Ramos, J.C. Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice. J. Exp. Med., 1994, 180, 95-109.
100. Wu, X.; Guo, R.; Wang, Y.; Cunningham, P.N. The role of ICAM-1 in endotoxin-induced acute renal failure. Am. J. Physiol. Renal Physiol., 2007, 293, F1262-1271.
101. Schmidt, E.P.; Yang, Y.; Janssen, W.J.; Gandjeva, A.; Perez, M.J.; Barthel, L.; Zemans, R.L.; Bowman, J.C.; Koyanagi, D.E.; Yunt, Z. X.; Smith, L.P.; Cheng, S.S.; Overdier, K.H.; Thompson, K.R.; Geraci, M.W.; Douglas, I.S.; Pearse, D.B.; Tuder, R.M. The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis. Nat. Med., 2012, 18, 1217-1223.
102. Wagner, J.G.; Driscoll, K.E.; Roth, R.A. Inhibition of pulmonary neutrophil trafficking during endotoxemia is dependent on the stimulus for migration. Am. J. Respir. Cell Mol. Biol., 1999, 20, 769-776.
103. Burns, A.R.; Doerschuk, C.M. Quantitation of L-selectin and CD18 expression on rabbit neutrophils during CD18-independent and CD18-dependent emigration in the lung. J. Immunol., 1994, 153, 3177-3188.
104. Guo, R.F.; Riedemann, N.C.; Laudes, I.J.; Sarma, V.J.; Kunkel, R. G.; Dilley, K.A.; Paulauskis, J.D.; Ward, P.A. Altered neutrophil trafficking during sepsis. J. Immunol., 2002, 169, 307-314.
105. Ibbotson, G.C.; Doig, C.; Kaur, J.; Gill, V.; Ostrovsky, L.; Fairhead, T.; Kubes, P. Functional alpha4-integrin: a newly identified pathway of neutrophil recruitment in critically ill septic patients. Nat. Med., 2001, 7, 465-470.
106. Cummings, C.J.; Martin, T.R.; Frevert, C.W.; Quan, J.M.; Wong, V. A.; Mongovin, S.M.; Hagen, T.R.; Steinberg, K.P.; Goodman, R. B. Expression and function of the chemokine receptors CXCR1 and CXCR2 in sepsis. J. Immunol., 1999, 162, 2341-2346.
107. Arraes, S.M.; Freitas, M.S.; da Silva, S.V.; de Paula Neto, H.A.; Alves-Filho, J.C.; Auxiliadora Martins, M.; Basile-Filho, A.; Tavares-Murta, B.M.; Barja-Fidalgo, C.; Cunha, F.Q. Impaired neutrophil chemotaxis in sepsis associates with GRK expression and inhibition of actin assembly and tyrosine phosphorylation. Blood, 2006, 108, 2906-2913.
108. Alves-Filho, J.C.; Freitas, A.; Souto, F.O.; Spiller, F.; Paula-Neto, H.; Silva, J.S.; Gazzinelli, R.T.; Teixeira, M.M.; Ferreira, S.H.; Cunha, F.Q. Regulation of chemokine receptor by Toll-like receptor 2 is critical to neutrophil migration and resistance to polymicrobial sepsis. Proc. Natl. Acad. Sci. USA, 2009, 106, 4018-4023.
109. Trevelin, S.C.; Alves-Filho, J.C.; Sonego, F.; Turato, W.; Nascimento, D.C.; Souto, F. O.; Cunha, T.M.; Gazzinelli, R.T.; Cunha, F.Q. Toll-like receptor 9 activation in neutrophils impairs chemotaxis and reduces sepsis outcome. Crit. Care Med., 2012, 40, 2631-2637.
110. Speyer, C.L.; Gao, H.; Rancilio, N.J.; Neff, T.A.; Huffnagle, G.B.; Sarma, J.V.; Ward, P.A. Novel chemokine responsiveness and mobilization of neutrophils during sepsis. Am. J. Pathol., 2004, 165, 2187-2196.
111. Souto, F.O.; Alves-Filho, J.C.; Turato, W.M.; Auxiliadora-Martins, M.; Basile-Filho, A.; Cunha, F.Q. Essential role of CCR2 in neutrophil tissue infiltration and multiple organ dysfunction in sepsis. Am. J. Respir. Crit. Care Med., 2011, 183, 234-242.
112. Yamada, M.; Kubo, H.; Kobayashi, S.; Ishizawa, K.; He, M.; Suzuki, T.; Fujino, N.; Kunishima, H.; Hatta, M.; Nishimaki, K.; Aoyagi, T.; Tokuda, K.; Kitagawa, M.; Yano, H.; Tamamura, H.; Fujii, N.; Kaku, M. The increase in surface CXCR4 expression on lung extravascular neutrophils and its effects on neutrophils during endotoxin-induced lung injury. Cell. Mol. Immunol., 2011, 8, 305-314.
113. Chen, S.; Lin, F.; Shin, M.E.; Wang, F.; Shen, L.; Hamm, H E. RACK1 regulates directional cell migration by acting on G betagamma at the interface with its effectors PLC beta and PI3K gamma. Mol. Biol. Cell, 2008, 19, 3909-3922.
114. Herrmann, J.M.; Bernardo, J.; Long, H. J.; Seetoo, K.; McMenamin, M.E.; Batista, E.L., Jr.; Van Dyke, T.E.; Simons, E. R. Sequential chemotactic and phagocytic activation of human polymorphonuclear neutrophils. Infect. Immun., 2007, 75, 3989-3998.
115. Kolls, J.; Xie, J.; LeBlanc, R.; Malinski, T.; Nelson, S.; Summer, W.; Greenberg, S.S. Rapid induction of messenger RNA for nitric oxide synthase II in rat neutrophils in vivo by endotoxin and its suppression by prednisolone. Proc. Soc. Exp. Biol. Med., 1994, 205, 220-229.
116. Tsukahara, Y.; Morisaki, T.; Horita, Y.; Torisu, M.; Tanaka, M. Expression of inducible nitric oxide synthase in circulating neutrophils of the systemic inflammatory response syndrome and septic patients. World J. Surg., 1998, 22, 771-777.
117. Fierro, I.M.; Nascimento-DaSilva, V.; Arruda, M.A.; Freitas, M. S.; Plotkowski, M.C.; Cunha, F.Q.; Barja-Fidalgo, C. Induction of NOS in rat blood PMN in vivo and in vitro: modulation by tyrosine kinase and involvement in bactericidal activity. J. Leukoc. Biol., 1999, 65, 508-514.
118. Sato, K.; Miyakawa, K.; Takeya, M.; Hattori, R.; Yui, Y.; Sunamoto, M.; Ichimori, Y.; Ushio, Y.; Takahashi, K. Immunohistochemical expression of inducible nitric oxide synthase (iNOS) in reversible endotoxic shock studied by a novel monoclonal antibody against rat iNOS. J. Leukoc. Biol., 1995, 57, 36-44.
119. Ferrer, R.; Artigas, A.; Suarez, D.; Palencia, E.; Levy, M.M.; Arenzana, A.; Perez, X.L.; Sirvent, J.M. Effectiveness of treatments for severe sepsis: a prospective, multicenter, observational study. Am. J. Respir. Crit. Care Med., 2009, 180, 861-866.
120. Kalil, A.C.; LaRosa, S.P. Effectiveness and safety of drotrecogin alfa (activated) for severe sepsis: a meta-analysis and metaregression. Lancet Infect. Dis, 2012, 12, 678-686.
121. Moilanen, E.; Vuorinen, P.; Kankaanranta, H.; Metsa-Ketela, T.; Vapaatalo, H. Inhibition by nitric oxide-donors of human polymorphonuclear leucocyte functions. Br. J. Pharmacol., 1993, 109, 852-858.
122. Rios-Santos, F.; Alves-Filho, J.C.; Souto, F.O.; Spiller, F.; Freitas, A.; Lotufo, C.M.; Soares, M.B.; Dos Santos, R.R.; Teixeira, M.M.; Cunha, F.Q. Down-regulation of CXCR2 on neutrophils in severe sepsis is mediated by inducible nitric oxide synthase-derived nitric oxide. Am. J. Respir. Crit. Care Med., 2007, 175, 490-497.
123. Clements, M.K.; Siemsen, D.W.; Swain, S.D.; Hanson, A.J.; Nelson-Overton, L.K.; Rohn, T.T.; Quinn, M.T. Inhibition of actin polymerization by peroxynitrite modulates neutrophil functional responses. J. Leukoc. Biol., 2003, 73, 344-355.
124. Li, L.; Bhatia, M.; Zhu, Y. Z.; Zhu, Y. C.; Ramnath, R.D.; Wang, Z. J.; Anuar, F.B.; Whiteman, M.; Salto-Tellez, M.; Moore, P.K. Hydrogen sulfide is a novel mediator of lipopolysaccharideinduced inflammation in the mouse. FASEB J., 2005, 19, 1196-1198.
125. Spiller, F.; Orrico, M.I.; Nascimento, D.C.; Czaikoski, P. G.; Souto, F. O.; Alves-Filho, J.C.; Freitas, A.; Carlos, D.; Montenegro, M.F.; Neto, A.F.; Ferreira, S.H.; Rossi, M.A.; Hothersall, J.S.; Assreuy, J.; Cunha, F. Q. Hydrogen sulfide improves neutrophil migration and survival in sepsis via K+ATP channel activation. Am. J. Respir. Crit. Care Med., 2010, 182, 360-368.
126. Dal-Secco, D.; Cunha, T.M.; Freitas, A.; Alves-Filho, J.C.; Souto, F.O.; Fukada, S.Y.; Grespan, R.; Alencar, N.M.; Neto, A.F.; Rossi, M.A.; Ferreira, S.H.; Hothersall, J.S.; Cunha, F.Q. Hydrogen sulfide augments neutrophil migration through enhancement of adhesion molecule expression and prevention of CXCR2 internalization: role of ATP-sensitive potassium channels. J. Immunol., 2008, 181, 4287-4298.
127. Meziani, F.; Delabranche, X.; Asfar, P.; Toti, F. Bench-to-bedside review: circulating microparticles--a new player in sepsis?. Crit. Care, 2010, 14, 236.
128. Nolan, S.; Dixon, R.; Norman, K.; Hellewell, P.; Ridger, V. Nitric oxide regulates neutrophil migration through microparticle formation. Am. J. Pathol., 2008, 172, 265-273.