Neutrophils and Intravascular Immunity in the Liver during Infection and Sterile Inflammation

Toxicologic Pathology

Volumn 40, Issue 2, 2012, Pages 157-165

  Mcdonald, Braedon ^a   Kubes, Paul ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

inflammation; liver; neutrophil; leukocyte trafficking

Indexed keywords

ANTIBIOTIC AGENT; BETA2 INTEGRIN; CD44V ANTIGEN; DROTRECOGIN; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; HISTONE; INTERLEUKIN 10; PADGEM PROTEIN; SELECTIN; SERINE PROTEINASE; TOLL LIKE RECEPTOR 4; VASCULAR CELL ADHESION MOLECULE 1;

AUTOIMMUNITY; CD8+ T LYMPHOCYTE; CELL DEATH; ENDOTOXEMIA; ESCHERICHIA COLI; FULMINANT HEPATIC FAILURE; HEPATITIS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LEUKOCYTE; LEUKOCYTE ROLLING; LIVER DISEASE; LIVER DYSFUNCTION; LIVER INJURY; LIVER SINUSOID; MICROVASCULATURE; MORTALITY; MULTIPLE ORGAN FAILURE; NEUTROPHIL; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; REVIEW; SEPSIS; SHOCK; WOUND HEALING;

ANIMALS; HEPATITIS; HUMANS; INFLAMMATION; LIVER; MICROVESSELS; NEUTROPHIL INFILTRATION; NEUTROPHILS;

EID: 84858787280     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623311427570     Document Type: Article

References (71)

1. Alves-Filho J. C. de Freitas A. Russo M. Cunha F. Q. (2006). Toll-like receptor 4 signaling leads to neutrophil migration impairment in polymicrobial sepsis. Crit Care Med 34, 461–70.
2. 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. (2009). Regulation of chemokine receptor by Toll-like receptor 2 is critical to neutrophil migration and resistance to polymicrobial sepsis. Proc Natl Acad Sci USA 106, 4018–23.
3. Andonegui G. Zhou H. Bullard D. Kelly M. M. Mullaly S. C. McDonald B. Long E. M. Robbins S. M. Kubes P. (2009). Mice that exclusively express TLR4 on endothelial cells can efficiently clear a lethal systemic gram-negative bacterial infection. J Clin Invest 119, 1921–30.
4. Bautista A. P. (1997). Chronic alcohol intoxication induces hepatic injury through enhanced macrophage inflammatory protein-2 production and intercellular adhesion molecule-1 expression in the liver. Hepatology 25, 335–42.
5. Beiter K. Wartha F. Albiger B. Normark S. Zychlinsky A. Henriques-Normark B. (2006). An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr Biol 16, 401–7.
6. Benacerraf B. Sebestyen M. M. Schlossman S. (1959). A quantitative study of the kinetics of blood clearance of P32-labelled Escherichia coli and Staphylococci by the reticuloendothelial system. J Exp Med 110, 27–48.
7. Bonder C. S. Ajuebor M. N. Zbytnuik L. D. Kubes P. Swain M. G. (2004). Essential role for neutrophil recruitment to the liver in concanavalin A-induced hepatitis. J Immunol 172, 45–53.
8. Bonder C. S. Norman M. U. Swain M. G. Zbytnuik L. D. Yamanouchi J. Santamaria P. Ajuebor M. Salmi M. Jalkanen S. Kubes P. (2005). Rules of recruitment for Th1 and Th2 lymphocytes in inflamed liver: A role for alpha-4 integrin and vascular adhesion protein-1. Immunity 23, 153–63.
9. Bone R.C. Balk R.A. Cerra F.B. Dellinger R.P. Fein A.M. Knaus W.A. Schein R.M. Sibbald W.J. (1992). Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 101, 1644–1655.
10. Brinkmann V. Reichard U. Goosmann C. Fauler B. Uhlemann Y. Weiss D. S. Weinrauch Y. Zychlinsky A. (2004). Neutrophil extracellular traps kill bacteria. Science 303, 1532–35.
11. Brown K. A. Brain S. D. Pearson J. D. Edgeworth J. D. Lewis S. M. Treacher D. F. (2006). Neutrophils in development of multiple organ failure in sepsis. Lancet 368, 157–69.
12. Buchanan J. T. Simpson A. J. Aziz R. K. Liu G. Y. Kristian S. A. Kotb M. Feramisco J. Nizet V. (2006). DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol 16, 396–400.
13. Carp H. (1982). Mitochondrial N-formylmethionyl proteins as chemoattractants for neutrophils. J Exp Med 155, 264–75.
14. Chen G. Y. Nuñez G. (2010). Sterile inflammation: Sensing and reacting to damage. Nat Rev Immunol 10, 826–37.
15. Christoffersson G. Henriksnäs J. Johansson L. Rolny C. Ahlström H. Caballero-Corbalan J. Segersvärd R. Permert J. Korsgren O. Carlsson P. O. Phillipson M. (2010). Clinical and experimental pancreatic islet transplantation to striated muscle: Establishment of a vascular system similar to that in native islets. Diabetes 59, 2569–78.
16. Clark S. R. Ma A. C. Tavener S. A. McDonald B. Goodarzi Z. Kelly M. M. Patel K. D. Chakrabarti S. McAvoy E. Sinclair G. D. Keys E. M. Allen-Vercoe E. Devinney R. Doig C. J. Green F. H. Kubes P. (2007). Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 13, 463–69.
17. Crispe I. N. (2009). The liver as a lymphoid organ. Annu Rev Immunol 27, 147–63.
18. Dellinger R. P. Levy M. Carlet J. Bion J. Parker M. Jaeschke R. Reinhart K. Angus D. C. Brun-Buisson C. Beale R. Calandra T. Dhainaut J. F. Gerlach H. Harvey M. Marini J. J. Marshall J. Ranieri M. Ramsay G. Sevransky J. Thompson B. T. Townsend S. Vender J. S. Zimmerman J. Vincent J. (2008). Surviving Sepsis Campaign: International guidelines for management of severe sepsis and septic shock: 2008. Crit Care Med, 36, 296–327.
19. Dhainaut J. F. Marin N. Mignon A. Vinsonneau C. (2001). Hepatic response to sepsis: interaction between coagulation and inflammatory processes. Crit Care Med 29, S42–47.
20. Dombrovskiy V. Y. Martin A. A. Sunderram J. Paz H. L. (2007). Rapid increase in hospitalization and mortality rates for severe sepsis in the United States: A trend analysis from 1993 to 2003. Crit Care Med 35, 1244–50.
21. Eigenbrod T. Park J. H. Harder J. Iwakura Y. Núñez G. (2008). Cutting edge: critical role for mesothelial cells in necrosis-induced inflammation through the recognition of IL-1 alpha released from dying cells. J Immunol 181, 8194–98.
22. Fox-Robichaud A. Kubes P. (2000). Molecular mechanisms of tumor necrosis factor alpha-stimulated leukocyte recruitment into the murine hepatic circulation. Hepatology 31, 1123–27.
23. Gaboury J. P. Kubes P. (1994). Reductions in physiologic shear rates lead to CD11/CD18-dependent, selectin-independent leukocyte rolling in vivo. Blood 83, 345–50.
24. Galper J. B. (1974). Mitochondrial protein synthesis in HeLa cells. J Cell Biol 60, 755–63.
25. Gregory S. H. Sagnimeni A. J. Wing E. J. (1996). Bacteria in the bloodstream are trapped in the liver and killed by immigrating neutrophils. J Immunol 157, 2514–20.
26. Gregory S. H. Wing E. J. (2002). Neutrophil-Kupffer cell interaction: A critical component of host defenses to systemic bacterial infections. J Leukoc Biol 72, 239–48.
27. Ibbotson G. C. Doig C. Kaur J. Gill V. Ostrovsky L. Fairhead T. Kubes P. (2001). Functional alpha4-integrin: A newly identified pathway of neutrophil recruitment in critically ill septic patients. Nat Med, 7, 465–70.
28. Jaeschke H. Farhood A. (1991). Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol 260, G355–62.
29. Jaeschke H. Farhood A. Fisher M. A. Smith C. W. (1996). Sequestration of neutrophils in the hepatic vasculature during endotoxemia is independent of beta 2 integrins and intercellular adhesion molecule-1. Shock 6, 351–56.
30. Jaeschke H. Farhood A. Smith C. W. (1990). Neutrophils contribute to ischemia/reperfusion injury in rat liver in vivo. FASEB J 4, 3355–59.
31. John B. Crispe I. N. (2004). Passive and active mechanisms trap activated CD8+ T cells in the liver. J Immunol 172, 5222–29.
32. Khan A. I. Heit B. Andonegui G. Colarusso P. Kubes P. (2005). Lipopolysaccharide: A p38 MAPK-dependent disrupter of neutrophil chemotaxis. Microcirculation 12, 421–32.
33. Kono H. Rock K. (2008). How dying cells alert the immune system to danger. Nat Rev Immunol 8, 279–89.
34. Kortgen A. Paxian M. Werth M. Recknagel P. Rauchfu F. Lupp A. Krenn C.G. Müller D. Claus R. A. Reinhart K. Settmacher U. Bauer M. (2009). Prospective assessment of hepatic function and mechanisms of dysfunction in the critically ill. Shock 32, 358–65.
35. Kreisel D. Nava R. G. Li W. Zinselmeyer B. H. Wang B. Lai J. Pless R. Gelman A. E. Krupnick A. S. Miller M. J. (2010). In vivo two-photon imaging reveals monocyte-dependent neutrophil extravasation during pulmonary inflammation. Proc Natl Acad Sci USA 107, 18073–78.
36. Kuligowski M. P. Kitching A. R. Hickey M. (2006). Leukocyte recruitment to the inflamed glomerulus: A critical role for platelet-derived P-selectin in the absence of rolling. J Immunol 176, 6991–99.
37. Lee W. Y. Kubes P. (2008). Leukocyte adhesion in the liver: Distinct adhesion paradigm from other organs. J Hepatol 48, 504–12.
38. Lekstrom-Himes J. A. Gallin J. I. (2000). Immunodeficiency diseases caused by defects in phagocytes. N Engl J Med 343, 1703–14.
39. Ley K. Gaehtgens P. Fennie C. Singer M. S. Lasky L. A. Rosen S.D. (1991). Lectin-like cell adhesion molecule 1 mediates leukocyte rolling in mesenteric venules in vivo. Blood 77, 2553–55.
40. Ley K. Laudanna C. Cybulsky M. Nourshargh S. (2007). Getting to the site of inflammation: The leukocyte adhesion cascade updated. Nat Rev Immunol 7, 678–89.
41. Li P. Li M. Lindberg M. R. Kennett M. J. Xiong N. Wang Y. (2010). PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med 207, 1853–62.
42. Liu Z. X. Han D. Gunawan B. Kaplowitz N. (2006). Neutrophil depletion protects against murine acetaminophen hepatotoxicity. Hepatology 43, 1220–30.
43. Mackay C. R. (2008). Moving targets: Cell migration inhibitors as new anti-inflammatory therapies. Nat Immunol 9, 988–98.
44. Martin G. S. Mannino D. M. Eaton S. Moss M. (2003). The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 348, 1546–54.
45. Martinez-Mier G. Toledo-Pereyra L. H. McDuffie J. E. Warner R. L. Ward P. A. (2001). Neutrophil depletion and chemokine response after liver ischemia and reperfusion. J Invest Surg 14, 99–107.
46. Massberg S. Grahl L. von Bruehl M. L. Manukyan D. Pfeiler S. Goosmann C. Brinkmann V. Lorenz M. Bidzhekov K. Khandagale A. B. Konrad I. Kennerknecht E. Reges K. Holdenrieder S. Braun S. Reinhardt C. Spannagl M. Preissner K. T. Engelmann B. (2010). Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 16, 887–96.
47. McDonald B. McAvoy E. F. Lam F. Gill V. de la Motte C. Savani R. C. Kubes P. (2008). Interaction of CD44 and hyaluronan is the dominant mechanism for neutrophil sequestration in inflamed liver sinusoids. J Exp Med 205, 915–27.
48. McDonald B. Pittman K. Menezes G. B. Hirota S. A. Slaba I. Waterhouse C. C. Beck P. L. Muruve D. A. Kubes P. (2010). Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330, 362–66.
49. Menezes G. B. Lee W. Y. Zhou H. Waterhouse C. C. Cara D. C. Kubes P. (2009). Selective down-regulation of neutrophil Mac-1 in endotoxemic hepatic microcirculation via IL-10. J Immunol 183, 7557–68.
50. Mizgerd J. P. Kubo H. Kutkoski G. J. Bhagwan S. D. Scharffetter-Kochanek K. Beaudet A. L. Doerschuk C. M. (1997). Neutrophil emigration in the skin, lungs, and peritoneum: Different requirements for CD11/CD18 revealed by CD18-deficient mice. J Exp Med 186, 1357–64.
51. Mizgerd J. P. Meek B. B. Kutkoski G. J. Bullard D. C. Beaudet A. L. Doerschuk C. M. (1996). Selectins and neutrophil traffic: Margination and Streptococcus pneumoniae-induced emigration in murine lungs. J Exp Med 184, 639–45.
52. Molnar R. G. Wang P. Ayala A. Ganey P. E. Roth R. A. Chaudry I. H. (1997). The role of neutrophils in producing hepatocellular dysfunction during the hyperdynamic stage of sepsis in rats. J Surg Res 73, 117–22.
53. Nathan C. (2006). Neutrophils and immunity: Challenges and opportunities. Nat Rev Immunol 6, 173–82.
54. Ng L. G. Qin J. S. Roediger B. Wang Y. Jain R. Cavanagh L. L. Smith A. L. Jones C. A. de Veer M. Grimbaldeston M. A. Meeusen E. N. Weninger W. (2011). Visualizing the neutrophil response to sterile tissue injury in mouse dermis reveals a three-phase cascade of events. J Investigative Dermatol 131, 2058–68.
55. Ohta Y. Imai Y. Matsura T. Kitagawa A. Yamada K. (2006). Preventive effect of neutropenia on carbon tetrachloride-induced hepatotoxicity in rats. J Appl Toxicol 26, 178–86.
56. Papayannopoulos V. Zychlinsky A. (2009). NETs: A new strategy for using old weapons. Trends Immunol 30, 513–21.
57. Petri B. Phillipson M. Kubes P. (2008). The physiology of leukocyte recruitment: An in vivo perspective. J Immunol 180, 6439–46.
58. Phillipson M. Heit B. Colarusso P. Liu L. Ballantyne C. M. Kubes P. (2006). Intraluminal crawling of neutrophils to emigration sites: A molecularly distinct process from adhesion in the recruitment cascade. J Exp Med 203, 2569–75.
59. Pilsczek F. H. Salina D. Poon K. K. Fahey C. Yipp B. G. Sibley C. D. Robbins S. M. Green F. H. Surette M. G. Sugai M. Bowden M. G. Hussain M. Zhang K. Kubes P. (2010). A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 185, 7413–25.
60. Segal A. W. (2005). How neutrophils kill microbes. Annu Rev Immunol 23, 197–223.
61. Shi C. Velázquez P. Hohl T. M. Leiner I. Dustin M. L. Pamer E. G. (2010). Monocyte trafficking to hepatic sites of bacterial infection is chemokine independent and directed by focal intercellular adhesion molecule-1 expression. J Immunol 184, 6266–74.
62. Smith C. W. Kishimoto T. K. Abbassi O. Hughes B. Rothlein R. McIntire L. V. Butcher E. Anderson D. C. Abbass O. (1991). Chemotactic factors regulate lectin adhesion molecule 1 (LECAM-1)-dependent neutrophil adhesion to cytokine-stimulated endothelial cells in vitro. J Clin Invest 87, 609–18.
63. Soehnlein O. Lindbom L. (2010). Phagocyte partnership during the onset and resolution of inflammation. Nat Rev Immunol 10, 427–39.
64. Takai S. Kimura K. Nagaki M. Satake S. Kakimi K. Moriwaki H. (2005). Blockade of neutrophil elastase attenuates severe liver injury in hepatitis B transgenic mice. J Virol 79, 15142–50.
65. von Andrian U. H. Chambers J. D. McEvoy L. M. Bargatze R. F. Arfors K. E. Butcher E. C. (1991). Two-step model of leukocyte-endothelial cell interaction in inflammation: Distinct roles for LECAM-1 and the leukocyte beta 2 integrins in vivo. Proc Natl Acad Sci USA 88, 7538–42.
66. Wong J. Johnston B. Lee S. S. Bullard D. C. Smith C. W. Beaudet A. L. Kubes P. (1997). A minimal role for selectins in the recruitment of leukocytes into the inflamed liver microvasculature. J Clin Invest 99, 2782–90.
67. Worthen G. S. Schwab B. Elson E. L. Downey G. P. (1989). Mechanics of stimulated neutrophils: Cell stiffening induces retention in capillaries. Science 245, 183–86.
68. Xu J. Zhang X. Pelayo R. Monestier M. Ammollo C. T. Semeraro F. Taylor F. B. Esmon N. L. Lupu F. Esmon C. T. (2009). Extracellular histones are major mediators of death in sepsis. Nat Med 15, 1318–21.
69. Yang C. W. Strong B. S. Miller M. J. Unanue E. R. (2010). Neutrophils influence the level of antigen presentation during the immune response to protein antigens in adjuvants. J Immunol 185, 2927–34.
70. Ye X. Ding J. Zhou X. Chen G. Liu S. F. (2008). Divergent roles of endothelial NF-kappaB in multiple organ injury and bacterial clearance in mouse models of sepsis. J Exp Med 205, 1303–15.
71. Zhang Q. Raoof M. Chen Y. Sumi Y. Sursal T. Junger W. Brohi K. Itagaki K. Hauser C. J. (2010). Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464, 104–7.