Cardiopulmonary Bypass during Cardiac Surgery Modulates Systemic Inflammation by Affecting Different Steps of the Leukocyte Recruitment Cascade

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Rossaint, Jan ^a   Berger, Christian ^a   van Aken, Hugo ^a   Scheld, Hans H ^a   Zahn, Peter K ^b   Rukosujew, Andreas ^a   Zarbock, Alexander ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PADGEM PROTEIN; PHOSPHOLIPASE C GAMMA2; PROTEIN KINASE B;

ADULT; AGED; ARTICLE; CARDIOPULMONARY BYPASS; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; IMMUNOMODULATION; INFLAMMATION; INTRACELLULAR SIGNALING; LEUKOCYTE FUNCTION; LEUKOCYTE MIGRATION; LEUKOCYTE MIGRATION INHIBITION; LEUKOCYTE RECRUITMENT; LEUKOCYTE ROLLING; MALE; MOLECULAR MECHANICS; NEUTROPHIL; OFF PUMP CORONARY SURGERY; UPREGULATION;

AGED; CELL SEPARATION; CORONARY ARTERY BYPASS; FEMALE; FLOW CYTOMETRY; HUMANS; LEUKOCYTES; MALE; PHOSPHOLIPASE C GAMMA; PHOSPHORYLATION; PROTEIN KINASES; SIGNAL TRANSDUCTION; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

EID: 84866535003     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045738     Document Type: Article

References (78)

1. Warren OJ, Smith AJ, Alexiou C, Rogers PL, Jawad N, et al. (2009) The inflammatory response to cardiopulmonary bypass: part 1-mechanisms of pathogenesis. Journal of cardiothoracic and vascular anesthesia 23: 223-231.
2. Paparella D, Yau TM, Young E, (2002) Cardiopulmonary bypass induced inflammation: pathophysiology and treatment. An update. European journal of cardio-thoracic surgery: official journal of the European Association for Cardio-thoracic Surgery 21: 232-244.
3. Asimakopoulos G, (2001) Systemic inflammation and cardiac surgery: an update. Perfusion 16: 353-360.
4. Landis RC, (2009) Redefining the systemic inflammatory response. Seminars in cardiothoracic and vascular anesthesia 13: 87-94.
5. Ben-Abraham R, Weinbroum AA, Dekel B, Paret G, (2003) Chemokines and the inflammatory response following cardiopulmonary bypass-a new target for therapeutic intervention?-A review. Paediatric anaesthesia 13: 655-661.
6. Braude S, Nolop KB, Fleming JS, Krausz T, Taylor KM, et al. (1986) Increased pulmonary transvascular protein flux after canine cardiopulmonary bypass. Association with lung neutrophil sequestration and tissue peroxidation. The American review of respiratory disease 134: 867-872.
7. Hind CR, Griffin JF, Pack S, Latchman YE, Drake HF, et al. (1988) Effect of cardiopulmonary bypass on circulating concentrations of leucocyte elastase and free radical activity. Cardiovascular research 22: 37-41.
8. Gillinov AM, Redmond JM, Zehr KJ, Wilson IC, Curtis WE, et al. (1994) Inhibition of neutrophil adhesion during cardiopulmonary bypass. The Annals of thoracic surgery 57: 126-133.
9. Dreyer WJ, Michael LH, West MS, Smith CW, Rothlein R, et al. (1991) Neutrophil accumulation in ischemic canine myocardium. Insights into time course, distribution, and mechanism of localization during early reperfusion. Circulation 84: 400-411.
10. Abdel-Rahman U, Margraf S, Aybek T, Logters T, Bitu-Moreno J, et al. (2007) Inhibition of neutrophil activity improves cardiac function after cardiopulmonary bypass. Journal of inflammation 4: 21.
11. Landis C, (2007) Pharmacologic strategies for combating the inflammatory response. The Journal of extra-corporeal technology 39: 291-295.
12. Ley K, Laudanna C, Cybulsky MI, Nourshargh S, (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7: 678-689.
13. Zarbock A, Ley K, McEver RP, Hidalgo A, (2011) Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood 118: 6743-6751.
14. Laudanna C, Bolomini-Vittori M, (2009) Integrin activation in the immune system. Wiley interdisciplinary reviews Systems biology and medicine 1: 116-127.
15. Alon R, Ley K, (2008) Cells on the run: shear-regulated integrin activation in leukocyte rolling and arrest on endothelial cells. Curr Opin Cell Biol 20: 525-532.
16. Zarbock A, Ley K, (2009) Neutrophil adhesion and activation under flow. Microcirculation 16: 31-42.
17. Zarbock A, Muller H, Kuwano Y, Ley K, (2009) PSGL-1-dependent myeloid leukocyte activation. J Leukoc Biol 86: 1119-1124.
18. Mueller H, Stadtmann A, Van Aken H, Hirsch E, Wang D, et al. (2010) Tyrosine kinase Btk regulates E-selectin-mediated integrin activation and neutrophil recruitment by controlling phospholipase C (PLC) gamma2 and PI3Kgamma pathways. Blood 115: 3118-3127.
19. Ley K, (2003) Arrest chemokines. Microcirculation 10: 289-295.
20. Kuwano Y, Spelten O, Zhang H, Ley K, Zarbock A, (2010) Rolling on E- or P-selectin induces the extended but not high-affinity conformation of LFA-1 in neutrophils. Blood 116: 617-624.
21. Rossaint J, Spelten O, Kassens N, Mueller H, Van Aken HK, et al. (2011) Acute loss of renal function attenuates slow leukocyte rolling and transmigration by interfering with intracellular signaling. Kidney international 80: 493-503.
22. Schnoor M, Lai FP, Zarbock A, Klaver R, Polaschegg C, et al. (2011) Cortactin deficiency is associated with reduced neutrophil recruitment but increased vascular permeability in vivo. The Journal of experimental medicine 208: 1721-1735.
23. Zarbock A, Abram CL, Hundt M, Altman A, Lowell CA, et al. (2008) PSGL-1 engagement by E-selectin signals through Src kinase Fgr and ITAM adapters DAP12 and FcR gamma to induce slow leukocyte rolling. J Exp Med 205: 2339-2347.
24. Mueller H, Stadtmann A, Van Aken H, Hirsch E, Wang D, et al. (2010) Tyrosine kinase Btk regulates E-selectin-mediated integrin activation and neutrophil recruitment by controlling phospholipase C (PLC) gamma2 and PI3Kgamma pathways. Blood 115: 3118-3127.
25. Zarbock A, Lowell CA, Ley K, (2007) Spleen tyrosine kinase Syk is necessary for E-selectin-induced alpha(L)beta(2) integrin-mediated rolling on intercellular adhesion molecule-1. Immunity 26: 773-783.
26. Forsyth KD, Levinsky RJ, (1990) Preparative procedures of cooling and re-warming increase leukocyte integrin expression and function on neutrophils. J Immunol Methods 128: 159-163.
27. Glasser L, Fiederlein RL, (1990) The effect of various cell separation procedures on assays of neutrophil function. A critical appraisal. Am J Clin Pathol 93: 662-669.
28. Kuijpers TW, Tool AT, van der Schoot CE, Ginsel LA, Onderwater JJ, et al. (1991) Membrane surface antigen expression on neutrophils: a reappraisal of the use of surface markers for neutrophil activation. Blood 78: 1105-1111.
29. Kunkel EJ, Dunne JL, Ley K, (2000) Leukocyte arrest during cytokine-dependent inflammation in vivo. J Immunol 164: 3301-3308.
30. Lewis SM, Treacher DF, Bergmeier L, Brain SD, Chambers DJ, et al. (2009) Plasma from patients with sepsis up-regulates the expression of CD49d and CD64 on blood neutrophils. American journal of respiratory cell and molecular biology 40: 724-732.
31. Lo Presti R, Canino B, Montana M, Ferrara F, Carollo C, et al. (2004) Polymorphonuclear leukocyte integrin profile in vascular atherosclerotic disease. Clinical hemorheology and microcirculation 30: 53-60.
32. Marsik C, Mayr F, Cardona F, Schaller G, Wagner OF, et al. (2004) Endotoxin down-modulates P-selectin glycoprotein ligand-1 (PSGL-1, CD162) on neutrophils in humans. Journal of clinical immunology 24: 62-65.
33. Kuwano Y, Spelten O, Zhang H, Ley K, Zarbock A, (2010) Rolling on E- or P-selectin induces the extended but not high-affinity conformation of LFA-1 in neutrophils. Blood 116: 617-624.
34. Zarbock A, Muller H, Kuwano Y, Ley K, (2009) PSGL-1-dependent myeloid leukocyte activation. Journal of leukocyte biology 86: 1119-1124.
35. Zarbock A, Kempf T, Wollert KC, Vestweber D, (2012) Leukocyte integrin activation and deactivation: novel mechanisms of balancing inflammation. Journal of molecular medicine 90: 353-359.
36. Stadtmann A, Brinkhaus L, Mueller H, Rossaint J, Bolomini-Vittori M, et al. (2011) Rap1a activation by CalDAG-GEFI and p38 MAPK is involved in E-selectin-dependent slow leukocyte rolling. Eur J Immunol 41: 2074-2085.
37. Lamy A, Devereaux PJ, Prabhakaran D, Taggart DP, Hu S, et al. (2012) Off-Pump or On-Pump Coronary-Artery Bypass Grafting at 30 Days. The New England journal of medicine 366: 1489-1497.
38. Murphy GJ, Angelini GD, (2004) Side effects of cardiopulmonary bypass: what is the reality? Journal of cardiac surgery 19: 481-488.
39. Marcantonio ER, Goldman L, Mangione CM, Ludwig LE, Muraca B, et al. (1994) A clinical prediction rule for delirium after elective noncardiac surgery. JAMA: the journal of the American Medical Association 271: 134-139.
40. Kumar AB, Suneja M, Bayman EO, Weide GD, Tarasi M, (2012) Association between postoperative acute kidney injury and duration of cardiopulmonary bypass: a meta-analysis. Journal of cardiothoracic and vascular anesthesia 26: 64-69.
41. Raja SG, Berg GA, (2007) Impact of off-pump coronary artery bypass surgery on systemic inflammation: current best available evidence. Journal of cardiac surgery 22: 445-455.
42. Asimakopoulos G, Kohn A, Stefanou DC, Haskard DO, Landis RC, et al. (2000) Leukocyte integrin expression in patients undergoing cardiopulmonary bypass. The Annals of thoracic surgery 69: 1192-1197.
43. Vestweber D, (2007) Adhesion and signaling molecules controlling the transmigration of leukocytes through endothelium. Immunol Rev 218: 178-196.
44. Klebanoff SJ, (2005) Myeloperoxidase: friend and foe. Journal of leukocyte biology 77: 598-625.
45. Hampton MB, Kettle AJ, Winterbourn CC, (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92: 3007-3017.
46. Vinten-Johansen J, (2004) Involvement of neutrophils in the pathogenesis of lethal myocardial reperfusion injury. Cardiovascular research 61: 481-497.
47. Wei M, Kuukasjarvi P, Laurikka J, Kaukinen S, Iisalo P, et al. (2003) Soluble adhesion molecules and myocardial injury during coronary artery bypass grafting. World journal of surgery 27: 140-144.
48. Hambsch J, Osmancik P, Bocsi J, Schneider P, Tarnok A, (2002) Neutrophil adhesion molecule expression and serum concentration of soluble adhesion molecules during and after pediatric cardiovascular surgery with or without cardiopulmonary bypass. Anesthesiology 96: 1078-1085.
49. Chesnutt BC, Smith DF, Raffler NA, Smith ML, White EJ, et al. (2006) Induction of LFA-1-dependent neutrophil rolling on ICAM-1 by engagement of E-selectin. Microcirculation 13: 99-109.
50. Block H, Herter JM, Rossaint J, Stadtmann A, Kliche S, et al. (2012) Crucial role of SLP-76 and ADAP for neutrophil recruitment in mouse kidney ischemia-reperfusion injury. The Journal of experimental medicine 209: 407-421.
51. Zarbock A, Ley K, (2008) Mechanisms and consequences of neutrophil interaction with the endothelium. Am J Pathol 172: 1-7.
52. Tellado JM, Christou NV, (1993) Activation state of polymorphonuclear leukocytes in surgical patients: characterization of surface receptor expression. Surgery 113: 624-630.
53. Rosenbloom AJ, Pinsky MR, Bryant JL, Shin A, Tran T, et al. (1995) Leukocyte activation in the peripheral blood of patients with cirrhosis of the liver and SIRS. Correlation with serum interleukin-6 levels and organ dysfunction. JAMA: the journal of the American Medical Association 274: 58-65.
54. Asimakopoulos G, Taylor KM, (1998) Effects of cardiopulmonary bypass on leukocyte and endothelial adhesion molecules. The Annals of thoracic surgery 66: 2135-2144.
55. Chishti AD, Shenton BK, Kirby JA, Baudouin SV, (2004) Neutrophil chemotaxis and receptor expression in clinical septic shock. Intensive care medicine 30: 605-611.
56. Rinder CS, Fontes M, Mathew JP, Rinder HM, Smith BR, (2003) Neutrophil CD11b upregulation during cardiopulmonary bypass is associated with postoperative renal injury. The Annals of thoracic surgery 75: 899-905.
57. Inoue T, Uchida T, Yaguchi I, Sakai Y, Takayanagi K, et al. (2003) Stent-induced expression and activation of the leukocyte integrin Mac-1 is associated with neointimal thickening and restenosis. Circulation 107: 1757-1763.
58. Schleiffenbaum B, Moser R, Patarroyo M, Fehr J, (1989) The cell surface glycoprotein Mac-1 (CD11b/CD18) mediates neutrophil adhesion and modulates degranulation independently of its quantitative cell surface expression. Journal of immunology 142: 3537-3545.
59. Vedder NB, Harlan JM, (1988) Increased surface expression of CD11b/CD18 (Mac-1) is not required for stimulated neutrophil adherence to cultured endothelium. The Journal of clinical investigation 81: 676-682.
60. Elliott MJ, Finn AH, (1993) Interaction between neutrophils and endothelium. The Annals of thoracic surgery 56: 1503-1508.
61. Orr Y, Taylor JM, Cartland S, Bannon PG, Geczy C, et al. (2007) Conformational activation of CD11b without shedding of L-selectin on circulating human neutrophils. Journal of leukocyte biology 82: 1115-1125.
62. May AE, Schmidt R, Kanse SM, Chavakis T, Stephens RW, et al. (2002) Urokinase receptor surface expression regulates monocyte adhesion in acute myocardial infarction. Blood 100: 3611-3617.
63. Rosenbloom AJ, Pinsky MR, Napolitano C, Nguyen TS, Levann D, et al. (1999) Suppression of cytokine-mediated beta2-integrin activation on circulating neutrophils in critically ill patients. Journal of leukocyte biology 66: 83-89.
64. Diacovo TG, Roth SJ, Buccola JM, Bainton DF, Springer TA, (1996) Neutrophil rolling, arrest, and transmigration across activated, surface-adherent platelets via sequential action of P-selectin and the beta 2-integrin CD11b/CD18. Blood 88: 146-157.
65. Faxon DP, Gibbons RJ, Chronos NA, Gurbel PA, Sheehan F, (2002) The effect of blockade of the CD11/CD18 integrin receptor on infarct size in patients with acute myocardial infarction treated with direct angioplasty: the results of the HALT-MI study. Journal of the American College of Cardiology 40: 1199-1204.
66. Simon DI, Xu H, Ortlepp S, Rogers C, Rao NK, (1997) 7E3 monoclonal antibody directed against the platelet glycoprotein IIb/IIIa cross-reacts with the leukocyte integrin Mac-1 and blocks adhesion to fibrinogen and ICAM-1. Arteriosclerosis, thrombosis, and vascular biology 17: 528-535.
67. Eltzschig HK, Carmeliet P, (2011) Hypoxia and inflammation. N Engl J Med 364: 656-665.
68. Liangos O, Domhan S, Schwager C, Zeier M, Huber PE, et al. (2010) Whole blood transcriptomics in cardiac surgery identifies a gene regulatory network connecting ischemia reperfusion with systemic inflammation. PloS one 5: e13658.
69. Cameron D, (1996) Initiation of white cell activation during cardiopulmonary bypass: cytokines and receptors. Journal of cardiovascular pharmacology 27 (Suppl 1):: S1-5.
70. Sniecinski RM, Chandler WL, (2011) Activation of the hemostatic system during cardiopulmonary bypass. Anesthesia and analgesia 113: 1319-1333.
71. Rinder CS, Bonan JL, Rinder HM, Mathew J, Hines R, et al. (1992) Cardiopulmonary bypass induces leukocyte-platelet adhesion. Blood 79: 1201-1205.
72. Rahman M, Zhang S, Chew M, Ersson A, Jeppsson B, et al. (2009) Platelet-derived CD40L (CD154) mediates neutrophil upregulation of Mac-1 and recruitment in septic lung injury. Annals of surgery 250: 783-790.
73. Cramer T, Yamanishi Y, Clausen BE, Forster I, Pawlinski R, et al. (2003) HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 112: 645-657.
74. Freyer DR, Boxer LA, Axtell RA, Todd RF 3rd (1988) Stimulation of human neutrophil adhesive properties by adenine nucleotides. Journal of immunology 141: 580-586.
75. Chen LW, Egan L, Li ZW, Greten FR, Kagnoff MF, et al. (2003) The two faces of IKK and NF-kappaB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion. Nature medicine 9: 575-581.
76. Montecucco F, Steffens S, Burger F, Da Costa A, Bianchi G, et al. (2008) Tumor necrosis factor-alpha (TNF-alpha) induces integrin CD11b/CD18 (Mac-1) up-regulation and migration to the CC chemokine CCL3 (MIP-1alpha) on human neutrophils through defined signalling pathways. Cellular signalling 20: 557-568.
77. Urner M, Herrmann IK, Buddeberg F, Schuppli C, Roth Z'graggen B, et al. (2012) Effects of blood products on inflammatory response in endothelial cells in vitro. PloS one 7: e33403.
78. Eckle T, Hartmann K, Bonney S, Reithel S, Mittelbronn M, et al. (2012) Adora2b-elicited Per2 stabilization promotes a HIF-dependent metabolic switch crucial for myocardial adaptation to ischemia. Nature medicine 18: 774-782.