Tissue-specific neutrophil recruitment into the lung, liver, and kidney

Journal of Innate Immunity

Volumn 5, Issue 4, 2013, Pages 348-357

  Rossaint, Jan ^a   Zarbock, Alexander ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

Inflammation; Kidney; Leukocyte; Liver; Lung; Neutrophil; Recruitment

Indexed keywords

ACUTE LUNG INJURY; BLOOD VESSEL PERMEABILITY; CELL POPULATION; ENDOTHELIUM CELL; GAS EXCHANGE; HUMAN; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; INTERSTITIUM; KIDNEY; LEUKOCYTE ACTIVATION; LIVER; LUNG; MACROPHAGE; MICROVASCULATURE; NEUTROPHIL; NEUTROPHIL RECRUITMENT; PRIORITY JOURNAL; REVIEW; TISSUE SPECIFICITY; VASCULARIZATION;

EID: 84879415574     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000345943     Document Type: Review

References (93)

1. Hanna S, Etzioni A: Leukocyte adhesion deficiencies. Ann NY Acad Sci 2012; 1250: 50-55.
2. Pinheiro da Silva F, Soriano FG: Neutrophils recruitment during sepsis: critical points and crossroads. Front Biosci 2009; 14: 4464-4476.
3. Ley K, Laudanna C, Cybulsky MI, Nourshargh S: Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7: 678-689.
4. Zarbock A, Ley K, McEver RP, Hidalgo A: Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood 2011; 118: 6743-6751.
5. Zarbock A, Lowell CA, Ley K: Spleen tyrosine kinase Syk is necessary for E-selectininduced alpha(L)beta(2) integrin-mediated rolling on intercellular adhesion molecule-1. Immunity 2007; 26: 773-783.
6. Kuwano Y, Spelten O, Zhang H, Ley K, Zarbock A: Rolling on E-or P-selectin induces the extended but not high-Affinity conformation of LFA-1 in neutrophils. Blood 2010; 116: 617-624.
7. Yago T, Shao B, Miner JJ, Yao L, Klopocki AG, Maeda K, Coggeshall KM, McEver RP: E-selectin engages PSGL-1 and CD44 through a common signaling pathway to induce integrin alphaLbeta2-mediated slow leukocyte rolling. Blood 2010; 116: 485-494.
8. Ley K: Arrest chemokines. Microcirculation 2003; 10: 289-295.
9. Colditz IG, Schneider MA, Pruenster M, Rot A: Chemokines at large: in-vivo mechanisms of their transport, presentation and clearance. Thromb Haemost 2007; 97: 688-693.
10. Smith ML, Olson TS, Ley K: CXCR2-And Eselectin-induced neutrophil arrest during inflammation in vivo. J Exp Med 2004; 200: 935-939.
11. Kunkel EJ, Ley K: Distinct phenotype of E-selectin-deficient mice. E-selectin is required for slow leukocyte rolling in vivo. Circ Res 1996; 79: 1196-1204.
12. Mueller H, Stadtmann A, Van Aken H, Hirsch E, Wang D, Ley K, Zarbock A: Tyrosine kinase Btk regulates E-selectin-mediated integrin activation and neutrophil recruitment by controlling phospholipase C (PLC) gamma2 and PI3Kgamma pathways. Blood 2010; 115: 3118-3127.
13. Woodfin A, Voisin MB, Nourshargh S: Recent developments and complexities in neutrophil transmigration. Curr Opin Hematol 2010; 17: 9-17.
14. Lacy P, Eitzen G: Control of granule exocytosis in neutrophils. Front Biosci 2008; 13: 5559-5570.
15. McDonald B, Urrutia R, Yipp BG, Jenne CN, Kubes P: Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host Microbe 2012; 12: 324-333.
16. Caudrillier A, Kessenbrock K, Gilliss BM, Nguyen JX, Marques MB, Monestier M, Toy P, Werb Z, Looney MR: Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest 2012; 122: 2661-2671.
17. Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD, Pittman K, Asaduzzaman M, Wu K, Meijndert HC, Malawista SE, de Boisfleury Chevance A, Zhang K, Conly J, Kubes P: Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 2012; 18: 1386-1393.
18. Zarbock A, Polanowska-Grabowska RK, Ley K: Platelet-neutrophil-interactions: linking hemostasis and inflammation. Blood Rev 2007; 21: 99-111.
19. Smyth SS, McEver RP, Weyrich AS, Morrell CN, Hoffman MR, Arepally GM, French PA, Dauerman HL, Becker RC: Platelet functions beyond hemostasis. J Thromb Haemost 2009; 7: 1759-1766.
20. Kornerup KN, Salmon GP, Pitchford SC, Liu WL, Page CP: Circulating platelet-neutrophil complexes are important for subsequent neutrophil activation and migration. J Appl Physiol 2010; 109: 758-767.
21. Cruz MA, Diacovo TG, Emsley J, Liddington R, Handin RI: Mapping the glycoprotein Ibbinding site in the von Willebrand factor A1 domain. J Biol Chem 2000; 275: 19098-19105.
22. Zaffran Y, Meyer SC, Negrescu E, Reddy KB, Fox JE: Signaling across the platelet adhesion receptor glycoprotein Ib-IX induces alpha IIbbeta 3 activation both in platelets and a transfected Chinese hamster ovary cell system. J Biol Chem 2000; 275: 16779-16787.
23. Ruggeri ZM: Mechanisms initiating platelet thrombus formation. Thromb Haemost 1997; 78: 611-616.
24. Romo GM, Dong JF, Schade AJ, Gardiner EE, Kansas GS, Li CQ, McIntire LV, Berndt MC, Lopez JA: The glycoprotein Ib-IX-V complex is a platelet counterreceptor for P-selectin. J Exp Med 1999; 190: 803-814.
25. Andrews RK, Berndt MC: Platelet physiology and thrombosis. Thromb Res 2004; 114: 447-453.
26. Wang Y, Sakuma M, Chen Z, Ustinov V, Shi C, Croce K, Zago AC, Lopez J, Andre P, Plow E, Simon DI: Leukocyte engagement of platelet glycoprotein Ibalpha via the integrin Mac-1 is critical for the biological response to vascular injury. Circulation 2005; 112: 2993-3000.
27. Martin TR, Frevert CW: Innate immunity in the lungs. Proc Am Thorac Soc 2005; 2: 403-411.
28. Doerschuk CM: Leukocyte trafficking in alveoli and airway passages. Respir Res 2000; 1: 136-140.
29. Grommes J, Soehnlein O: Contribution of neutrophils to acute lung injury. Mol Med 2011; 17: 293-307.
30. Kuebler WM, Goetz AE: The marginated pool. Eur Surg Res 2002; 34: 92-100.
31. Wiggs BR, English D, Quinlan WM, Doyle NA, Hogg JC, Doerschuk CM: Contributions of capillary pathway size and neutrophil deformability to neutrophil transit through rabbit lungs. J Appl Physiol 1994; 77: 463-470.
32. Matthay MA, Ware LB, Zimmerman GA: The acute respiratory distress syndrome. J Clin Invest 2012; 122: 2731-2740.
33. Abraham E: Neutrophils and acute lung injury. Crit Care Med 2003; 31:S195-S199.
34. Abraham E, Carmody A, Shenkar R, Arcaroli J: Neutrophils as early immunologic effectors in hemorrhage-or endotoxemia-induced acute lung injury. Am J Physiol Lung Cell Mol Physiol 2000; 279:L1137-L1145.
35. Tanaka H, Nishino M, Dahms TE: Physiologic responses to small emboli and hemodynamic effects of changes in deformability of polymorphonuclear leukocytes in isolated rabbit lung. Microvasc Res 2002; 63: 81-90.
36. Drost EM, MacNee W: Potential role of IL-8, platelet-Activating factor and TNF-Alpha in the sequestration of neutrophils in the lung: effects on neutrophil deformability, adhesion receptor expression, and chemotaxis. Eur J Immunol 2002; 32: 393-403.
37. Worthen GS, Schwab B 3rd, Elson EL, Downey GP: Mechanics of stimulated neutrophils: cell stiffening induces retention in capillaries. Science 1989; 245: 183-186.
38. Bhatia M, Zemans RL, Jeyaseelan S: Role of chemokines in the pathogenesis of acute lung injury. Am J Respir Cell Mol Biol 2012; 46: 566-572.
39. Wang J, Nikrad MP, Travanty EA, Zhou B, Phang T, Gao B, Alford T, Ito Y, Nahreini P, Hartshorn K, Wentworth D, Dinarello CA, Mason RJ: Innate immune response of human alveolar macrophages during influenza A infection. PLoS One 2012; 7:e29879.
40. Zarbock A, Distasi MR, Smith E, Sanders JM, Kronke G, Harry BL, von Vietinghoff S, Buscher K, Nadler JL, Ley K: Improved survival and reduced vascular permeability by eliminating or blocking 12/15-lipoxygenase in mouse models of acute lung injury (ALI). J Immunol 2009; 183: 4715-4722.
41. Rossaint J, Nadler JL, Ley K, Zarbock A: Eliminating or blocking 12/15-lipoxygenase reduces neutrophil recruitment in mouse models of acute lung injury. Crit Care 2012; 16:R166.
42. Miller EJ, Cohen AB, Matthay MA: Increased interleukin-8 concentrations in the pulmonary edema fluid of patients with acute respiratory distress syndrome from sepsis. Crit Care Med 1996; 24: 1448-1454.
43. Kurdowska A, Noble JM, Grant IS, Robertson CR, Haslett C, Donnelly SC: Anti-interleukin-Autoantibodies in patients at risk for acute respiratory distress syndrome. Crit Care Med 2002; 30: 2335-2337.
44. Quinton LJ, Nelson S, Zhang P, Boe DM, Happel KI, Pan W, Bagby GJ: Selective transport of cytokine-induced neutrophil chemoattractant from the lung to the blood facilitates pulmonary neutrophil recruitment. Am J Physiol Lung Cell Mol Physiol 2004; 286:L465-L472.
45. Schmidt EP, Yang Y, Janssen WJ, Gandjeva A, Perez MJ, Barthel L, Zemans RL, Bowman JC, Koyanagi DE, Yunt ZX, Smith LP, Cheng SS, Overdier KH, Thompson KR, Geraci MW, Douglas IS, Pearse DB, Tuder RM: The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis. Nat Med 2012, E-pub ahead of time.
46. Handel TM, Johnson Z, Crown SE, Lau EK, Proudfoot AE: Regulation of protein function by glycosaminoglycans-As exemplified by chemokines. Annu Rev Biochem 2005; 74: 385-410.
47. Das ST, Rajagopalan L, Guerrero-Plata A, Sai J, Richmond A, Garofalo RP, Rajarathnam K: Monomeric and dimeric CXCL8 are both essential for in vivo neutrophil recruitment. PLoS One 2010; 5:e11754.
48. Belperio JA, Keane MP, Lynch JP 3rd, Strieter RM: The role of cytokines during the pathogenesis of ventilator-Associated and ventilator-induced lung injury. Semin Respir Crit Care Med 2006; 27: 350-364.
49. Strieter RM, Keane MP, Burdick MD, Sakkour A, Murray LA, Belperio JA: The role of CXCR2/CXCR2 ligands in acute lung injury. Curr Drug Targets Inflamm Allergy 2005; 4: 299-303.
50. Stadtmann A, Zarbock A: CXCR2: from bench to bedside. Front Immunol 2012; 3: 263.
51. Zarbock A, Allegretti M, Ley K: Therapeutic inhibition of CXCR2 by Reparixin attenuates acute lung injury in mice. Br J Pharmacol 2008; 155: 357-364.
52. Reutershan J, Morris MA, Burcin TL, Smith DF, Chang D, Saprito MS, Ley K: Critical role of endothelial CXCR2 in LPS-induced neutrophil migration into the lung. J Clin Invest 2006; 116: 695-702.
53. Konrad FM, Reutershan J: CXCR2 in acute lung injury. Mediators Inflamm 2012; 2012: 740987.
54. Mulligan MS, Miyasaka M, Ward PA: Protective effects of combined adhesion molecule blockade in models of acute lung injury. Proc Assoc Am Phys 1996; 108: 198-208.
55. Mulligan MS, Warner RL, Rittershaus CW, Thomas LJ, Ryan US, Foreman KE, Crouch LD, Till GO, Ward PA: Endothelial targeting and enhanced antiinflammatory effects of complement inhibitors possessing sialyl Lewisx moieties. J Immunol 1999; 162: 4952-4959.
56. Mizgerd JP, Meek BB, Kutkoski GJ, Bullard DC, Beaudet AL, Doerschuk CM: Selectins and neutrophil traffic: margination and Streptococcus pneumoniae-induced emigration in murine lungs. J Exp Med 1996; 184: 639-645.
57. Ganter MT, Roux J, Miyazawa B, Howard M, Frank JA, Su G, Sheppard D, Violette SM, Weinreb PH, Horan GS, Matthay MA, Pittet JF: Interleukin-1beta causes acute lung injury via alphavbeta5 and alphavbeta6 integrindependent mechanisms. Circ Res 2008; 102: 804-812.
58. Xu J, Gao XP, Ramchandran R, Zhao YY, Vogel SM, Malik AB: Nonmuscle myosin lightchain kinase mediates neutrophil transmigration in sepsis-induced lung inflammation by activating beta2 integrins. Nat Immunol 2008; 9: 880-886.
59. Mizgerd JP, Kubo H, Kutkoski GJ, Bhagwan SD, Scharffetter-Kochanek K, Beaudet AL, Doerschuk CM: Neutrophil emigration in the skin, lungs, and peritoneum: different requirements for CD11/CD18 revealed by CD18-deficient mice. J Exp Med 1997; 186: 1357-1364.
60. Hellewell PG, Young SK, Henson PM, Worthen GS: Disparate role of the beta 2-integrin CD18 in the local accumulation of neutrophils in pulmonary and cutaneous inflammation in the rabbit. Am J Respir Cell Mol Biol 1994; 10: 391-398.
61. Zarbock A, Singbartl K, Ley K: Complete reversal of acid-induced acute lung injury by blocking of platelet-neutrophil aggregation. J Clin Invest 2006; 116: 3211-3219.
62. Huang JS, Ramamurthy SK, Lin X, Le Breton GC: Cell signalling through thromboxane A2 receptors. Cell Signal 2004; 16: 521-533.
63. Grommes J, Alard JE, Drechsler M, Wantha S, Morgelin M, Kuebler WM, Jacobs M, von Hundelshausen P, Markart P, Wygrecka M, Preissner KT, Hackeng TM, Koenen RR, Weber C, Soehnlein O: Disruption of plateletderived chemokine heteromers prevents neutrophil extravasation in acute lung injury. Am J Respir Crit Care Med 2012; 185: 628-636.
64. Wong J, Johnston B, Lee SS, Bullard DC, Smith CW, Beaudet AL, Kubes P: A minimal role for selectins in the recruitment of leukocytes into the inflamed liver microvasculature. J Clin Invest 1997; 99: 2782-2790.
65. Lalor PF, Shields P, Grant A, Adams DH: Recruitment of lymphocytes to the human liver. Immunol Cell Biol 2002; 80: 52-64.
66. Scoazec JY, Feldmann G: The cell adhesion molecules of hepatic sinusoidal endothelial cells. J Hepatol 1994; 20: 296-300.
67. Steinhoff G, Behrend M, Schrader B, Duijvestijn AM, Wonigeit K: Expression patterns of leukocyte adhesion ligand molecules on human liver endothelia. Lack of ELAM-1 and CD62 inducibility on sinusoidal endothelia and distinct distribution of VCAM-1, ICAM-1, ICAM-2, and LFA-3. Am J Pathol 1993; 142: 481-488.
68. Fox-Robichaud A, Kubes P: Molecular mechanisms of tumor necrosis factor alphastimulated leukocyte recruitment into the murine hepatic circulation. Hepatology 2000; 31: 1123-1127.
69. McDonald B, Kubes P: Neutrophils and intravascular immunity in the liver during infection and sterile inflammation. Toxicol Pathol 2012; 40: 157-165.
70. DeLeve LD: Hepatic microvasculature in liver injury. Semin Liver Dis 2007; 27: 390-400.
71. Wisse E, De Zanger RB, Charels K, Van Der Smissen P, McCuskey RS: The liver sieve: considerations concerning the structure and function of endothelial fenestrae, the sinusoidal wall and the space of Disse. Hepatology 1985; 5: 683-692.
72. Scoazec JY, Racine L, Couvelard A, Flejou JF, Feldmann G: Endothelial cell heterogeneity in the normal human liver acinus: in situ immunohistochemical demonstration. Liver 1994; 14: 113-123.
73. McDonald B, McAvoy EF, Lam F, Gill V, de la Motte C, Savani RC, Kubes P: Interaction of CD44 and hyaluronan is the dominant mechanism for neutrophil sequestration in inflamed liver sinusoids. J Exp Med 2008; 205: 915-927.
74. Li X, Klintman D, Liu Q, Sato T, Jeppsson B, Thorlacius H: Critical role of CXC chemokines in endotoxemic liver injury in mice. J Leukocyte Biol 2004; 75: 443-452.
75. Patrick AL, Rullo J, Beaudin S, Liaw P, Fox-Robichaud AE: Hepatic leukocyte recruitment in response to time-limited expression of TNF-Alpha and IL-1beta. Am J Physiol Gastrointest Liver Physiol 2007; 293:G663-G672.
76. McDonald B, Pittman K, Menezes GB, Hirota SA, Slaba I, Waterhouse CC, Beck PL, Muruve DA, Kubes P: Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 2010; 330: 362-366.
77. Schlayer HJ, Laaff H, Peters T, Woort-Menker M, Estler HC, Karck U, Schaefer HE, Decker K: Involvement of tumor necrosis factor in endotoxin-triggered neutrophil adherence to sinusoidal endothelial cells of mouse liver and its modulation in acute phase. J Hepatol 1988; 7: 239-249.
78. Bajt ML, Farhood A, Jaeschke H: Effects of CXC chemokines on neutrophil activation and sequestration in hepatic vasculature. Am J Physiol Gastrointest Liver Physiol 2001; 281:G1188-G1195.
79. Croner RS, Hoerer E, Kulu Y, Hackert T, Gebhard MM, Herfarth C, Klar E: Hepatic platelet and leukocyte adherence during endotoxemia. Crit Care 2006; 10:R15.
80. Laschke MW, Dold S, Menger MD, Jeppsson B, Thorlacius H: Platelet-dependent accumulation of leukocytes in sinusoids mediates hepatocellular damage in bile duct ligationinduced cholestasis. Br J Pharmacol 2008; 153: 148-156.
81. Li L, Huang L, Sung SS, Vergis AL, Rosin DL, Rose CE Jr, Lobo PI, Okusa MD: The chemokine receptors CCR2 and CX3CR1 mediate monocyte/macrophage trafficking in kidney ischemia-reperfusion injury. Kidney Int 2008; 74: 1526-1537.
82. Block H, Herter JM, Rossaint J, Stadtmann A, Kliche S, Lowell CA, Zarbock A: Crucial role of SLP-76 and ADAP for neutrophil recruitment in mouse kidney ischemia-reperfusion injury. J Exp Med 2012; 209: 407-421.
83. Kelly KJ, Williams WW Jr, Colvin RB, Meehan SM, Springer TA, Gutierrez-Ramos JC, Bonventre JV: Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury. J Clin Invest 1996; 97: 1056-1063.
84. Tadagavadi RK, Reeves WB: Renal dendritic cells ameliorate nephrotoxic acute kidney injury. J Am Soc Nephrol 2010; 21: 53-63.
85. Singbartl K, Ley K: Protection from ischemia-reperfusion induced severe acute renal failure by blocking E-selectin. Crit Care Med 2000; 28: 2507-2514.
86. Singbartl K, Green SA, Ley K: Blocking Pselectin protects from ischemia/reperfusioninduced acute renal failure. FASEB J 2000; 14: 48-54.
87. Singbartl K, Forlow SB, Ley K: Platelet, but not endothelial, P-selectin is critical for neutrophil-mediated acute postischemic renal failure. FASEB J 2001; 15: 2337-2344.
88. Rouschop KM, Roelofs JJ, Claessen N, da Costa Martins P, Zwaginga JJ, Pals ST, Weening JJ, Florquin S: Protection against renal ischemia reperfusion injury by CD44 disruption. J Am Soc Nephrol 2005; 16: 2034-2043.
89. Awad AS, Rouse M, Huang L, Vergis AL, Reutershan J, Cathro HP, Linden J, Okusa MD: Compartmentalization of neutrophils in the kidney and lung following acute ischemic kidney injury. Kidney Int 2009; 75: 689-698.
90. Kitching AR, Kuligowski MP, Hickey MJ: In vivo imaging of leukocyte recruitment to glomeruli in mice using intravital microscopy. Methods Mol Biol 2009; 466: 109-117.
91. Kuligowski MP, Kitching AR, Hickey MJ: Leukocyte recruitment to the inflamed glomerulus: a critical role for platelet-derived P-selectin in the absence of rolling. J Immunol 2006; 176: 6991-6999.
92. Chung AC, Lan HY: Chemokines in renal injury. J Am Soc Nephrol 2011; 22: 802-809.
93. Devi S, Kuligowski MP, Kwan RY, Westein E, Jackson SP, Kitching AR, Hickey MJ: Platelet recruitment to the inflamed glomerulus occurs via an alphaIIbbeta3/GPVI-dependent pathway. Am J Pathol 2010; 177: 1131-1142.