Leukocyte apoptosis and its significance in sepsis and shock

Journal of Leukocyte Biology

Volumn 78, Issue 2, 2005, Pages 325-337

  Wesche, Doreen E ^a   Lomas Neira, Joanne L ^a   Perl, Mario ^a   Chung, Chun Shiang ^a   Ayala, Alfred ^a,b  

^a BROWN UNIVERSITY   (United States)

^b RHODE ISLAND HOSPITAL   (United States)

Author keywords

Death receptor pathway; Human; Immune and organ dysfunction; Mice; Mitochondrial pathway

Indexed keywords

ADRENOMEDULLIN; CASPASE INHIBITOR; CD14 ANTIGEN; COMPLEMENT COMPONENT C5A; CYTOKINE; CYTOKINE RESPONSE MODIFIER A; DEATH RECEPTOR; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FLICE INHIBITORY PROTEIN; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1; INTERLEUKIN 6; MYC PROTEIN; PROTEIN BAK; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; PROTEIN MCL 1; PROTEIN P35; PROTEINASE INHIBITOR; SMALL INTERFERING RNA; STEROID; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADULT RESPIRATORY DISTRESS SYNDROME; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; BURN; CANCER; CONTROLLED STUDY; CRITICAL ILLNESS; CYSTIC FIBROSIS; DENDRITIC CELL; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; ENZYME INHIBITION; EPITHELIUM CELL; GENE OVEREXPRESSION; INFECTION SENSITIVITY; INJURY; LEUKOCYTE; LYMPHOCYTE; MACROPHAGE; MITOCHONDRION; MORTALITY; MOUSE; MULTIPLE ORGAN FAILURE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; REVIEW; SALMONELLA TYPHIMURIUM; SEPSIS; SEPTIC SHOCK; STROKE; SURVIVAL; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

ANIMALS; APOPTOSIS; CASPASES; DENDRITIC CELLS; ENDOTHELIAL CELLS; ENZYME INHIBITORS; FAS LIGAND PROTEIN; HUMANS; LEUKOCYTES; MEMBRANE GLYCOPROTEINS; MICE; MULTIPLE ORGAN FAILURE; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, SMALL INTERFERING; SEPSIS; SHOCK, SEPTIC; STEROIDS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 23044477087     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0105017     Document Type: Review

References (164)

1. Angus, D. C., Linde-Zwirble, W. T., Lidicker, J., Clermont, G., Carcillo, J., Pinsky, M. R. (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29, 1303-1310.
2. van den Berghe, G., Wouters, P., Weekers, F., Verwaest, C., Bruyninckx, F., Schetz, M., Vlasselaers, D., Ferdinande, P., Lauwers, P., Bouillon, R. (2001) Intensive insulin therapy in critically ill patients. N. Engl. J. Med. 345, 1359-1367.
3. Annane, D., Sebille, V., Charpentier, C., Bollaert, P-E., Francois, B., Korach, J-M., Capellier, G., Cohen, Y., Azoulay, E., Troche, G., Chaumet-Riffaut, P., Bellissant, E. (2002) Effect of treatment with low doses of hydrocortisone and fludrocortisone on mortality in patients with septic shock. JAMA 288, 862-871.
4. Szabo, G., Romics, L., Frendl, G. (2002) Liver in sepsis and systemic inflammatory response syndrome. Clin. Liver Dis. 6, 1045-1066.
5. Deitch, E. A. (1998) Animal models of sepsis and shock: a review and lessons learned. Shock 9, 1-11.
6. Cerra, F. B. (1989) Hypermetabolism-organ failure syndrome: s metabolic response to injury. Crit. Care Clin. 5, 289-302.
7. Groeneveld, A. B., Bronsveld, W., Thijs, L. G. (1986) Hemodynamic determinants of mortality in human septic shock. Surgery 99, 140-153.
8. Yang, S., Chung, C. S., Ayala, A., Chaudry, I. H., Wang, P. (2002) Differential alterations in cardiovascular responses during the progression of polymicrobial sepsis in the mouse. Shock 17, 55-60.
9. Meakins, J. L., Pietsch, J. B., Bubenick, O., Kelly, R., Rode, H., Gordon, J., MacLean, L. D. (1977) Delayed hypersensitivity: indicator of acquired failure of host defenses in sepsis and trauma. Ann. Surg. 186, 241-250.
10. Pietsch, J. B., Meakins, J. L., MacLean, L. D. (1977) The delayed hypersensitivity response: application in clinical surgery. Surgery 82, 349-355.
11. Ayala, A., Lomas, J. L., Grutkoski, P. S., Chung, C. S. (2003) Pathological aspects of apoptosis in severe sepsis and shock? Int. J. Biochem. Cell Biol. 35, 7-15.
12. Oberholzer, C., Oberholzer, A., Clare-Salzler, M., Moldawer, L. L. (2001) Apoptosis in sepsis: a new target for therapeutic exploration. FASEB J. 15, 879-892.
13. Chaudry, I. H., Ayala, A., Singh, G., Wang, P., Hauptman, J. G. (1993) Rodent models of endotoxemia and sepsis. In Pathophysiology of Shock, Sepsis and Organ Failure (G. Schlag and H. Redl, eds.), Berlin, Springer-Verlag, 1048-1059.
14. Chaudry, I. H., Wichterman, K. A., Baue, A. E. (1979) Effect of sepsis on tissue adenine nucleotide levels. Surgery 85, 205-211.
15. Wichterman, K. A., Baue, A. E., Chaudry, I. H. (1980) Sepsis and septic shock-a review of laboratory models and a proposal. J. Surg. Res. 29, 189-201.
16. Turnbull, I. R., Javadi, P., Buchman, T. G., Hotchkiss, R. S., Karl, I. E., Coopersmith, C. M. (2004) Antibiotics improve survival in sepsis independent of injury severity but do not change mortality in mice with markedly elevated interleukin 6 levels. Shock 21, 121-125.
17. Newcomb, D., Bolgos, G., Green, L., Remick, D. G. (1998) Antibiotic treatment influences outcome in murine sepsis: mediators of increased morbidity. Shock 10, 110-117.
18. Chung, C. S., Song, G. Y., Lomas, J., Simms, H. H., Chaudry, I. H., Ayala, A. (2003) Inhibition of Fas/Fas ligand signaling improves septic survival: differential effects on macrophage apoptotic and functional capacity. J. Leukoc. Biol. 74, 344-351.
19. Chung, C. S., Yang, S. L., Song, G. Y., Lomas, J., Wang, P., Simms, H. H., Chaudry, I. H., Ayala, A. (2001) Inhibition of Fas signaling prevents hepatic injury and improves organ blood flow. Surgery 130, 339-345.
20. Ayala, A., Evans, T. A., Chaudry, I. H. (1998) Does hepatocellular injury in sepsis involve apoptosis? J. Surg. Res. 76, 165-173.
21. Hotchkiss, R. S., Swanson, P. E., Freeman, B. D., Tinsley, K. W., Cobb, J. P., Matuschak, G. M., Buchman, T. G., Karl, I. E. (1999) Apoptotic cell death in patients with sepsis, shock and multiple organ dysfunction. Crit. Care Med. 27, 1230-1251.
22. Roth, E., Hanspeter, P. (2004) IFN-γ promotes Fas ligand- and perforin-mediated liver cell destruction by cytotoxic CD8 T cells. J. Immunol. 172, 1588-1594.
23. Peter, M. E., Krammer, P. H. (2003) The CD95 (APO-1/Fas) DISC and beyond. Cell Death Differ. 10, 26-35.
24. Danial, N. N., Korsmeyer, S. J. (2004) Cell death: critical control points. Cell 116, 205-219.
25. Strasser, A., O'Connor, L., Dixit, V. M. (2000) Apoptosis signaling. Annu. Rev. Biochem. 69, 217-245.
26. Thorburn, A. (2004) Death receptor-induced cell killing. Cell. Signal. 16, 139-144.
27. Krammer, P. H. (1999) CD95 (APO-1/Fas)-mediated apoptosis: live and let die. Adv. Immunol. 71, 163-210.
28. Janeway Jr., C. A. (2001) How the immune system works to protect the host from infection: a personal view. Proc. Natl. Acad. Sci. USA 98, 7461-7468.
29. Mica, L., Harter, L., Trentz, O., Keel, M. (2004) Endotoxin reduces CD95-induced neutrophil apoptosis by cIAP-2-mediated caspase 3 degradation. J. Am. Coll. Surg. 199, 595-602.
30. Power, C. P., Wang, J. H., Manning, B., Kell, M. R., Aherne, N. F., Wu, Q. D., Redmond, H. P. (2004) Bacterial lipoprotein delays apoptosis in human neutrophils through inhibition of caspase-3 activity: regulatory roles for CD14 and TLR-2. J. Immunol. 173, 5229-5237.
31. Bannerman, D. D., Eiting, K. T., Winn, R. K., Harlan, J. M. (2004) FLICE-like inhibitory protein (FLIP) protects against apoptosis and suppresses NF-κB activation induced by bacterial lipopolysaccharide. Am. J. Pathol. 165, 1423-1431.
32. Krammer, P. H. (2000) CD95's deadly mission in the immune system. Nature 407, 789-795.
33. Oyadomari, S., Mori, M. (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11, 381-389.
34. Nakagawa, T., Zhu, H., Morishima, N., Li, E., Yanker, B. A., Yuan, J. (2000) Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-β. Nature 403, 98-103.
35. Stahelin, B.J., Marti, U., Solioz, M., Zimmerman, H., Reichen, J. (1998) False positive staining in the TUNEL assay to detect apoptosis in liver and intestines is caused by endogenous nucleases and inhibited by diethyl pyrocarbonate. Mol. Pathol. 51, 204-208.
36. Hotchkiss, R. S., Swanson, P. E., Knudson, C. M., Chang, K. C., Cobb, J. P., Osborne, D. F., Zollner, K. M., Buchman, T. G., Korsmeyer, S. J., Karl, I. E. (1999) Overexpression of Bcl-2 in transgenic mice decreases apoptosis and improves survival in sepsis. J. Immunol. 162, 4148-4156.
37. Mahidhara, R., Billiar, T. (2000) Apoptosis in sepsis. Crit. Care Med. 28, N105-N113.
38. Ayala, A., Herdon, C. D., Lehman, D. L., DeMaso, C. M., Ayala, C. A., Chaudry, I. H. (1995) The induction of accelerated thymic programmed cell death during polymicrobial sepsis: control by corticosteroids but not tumor necrosis factor. Shock 3, 259-267.
39. Ayala, A., Xu, Y. X., Chung, C. S., Chaudry, I. H. (1999) Does Fas ligand or endotoxin contribute to thymic apoptosis during polymicrobial sepsis? Shock 11, 211-217.
40. Cobb, J. P., Buchman, T. G., Chang, K., Qui, Y., Laubach, V. E., Hotchkiss, R. S. (1999) Inducible nitric oxide synthase (iNOS) gene deficiency increases the mortality of sepsis in mice. Surgery 126, 438-442.
41. Chung, C. S., Chaudry, I. H., Ayala, A. (2000) The apoptotic response of the lymphoid immune system to trauma, shock and sepsis. In Yearbook of Intensive Care and Emergency Medicine: 2000 (J-L. Vincent, ed.), Berlin, Spinger-Verlag, 27-40.
42. Guo, R-F., Huber-Lang, M., Wang, X., Sarma, V., Padgaonkar, V. A., Craig, R. A., Riedemann, N. C., McClintock, S. D., Hlaing, T., Shi, M. M., Ward, P. A. (2000) Protective effects of anti-C5a in sepsis-induced thymocyte apoptosis. J. Clin. Invest. 106, 1271-1280.
43. Chung, C. S., Wang, W., Chaudry, I. H., Ayala, A. (2001) Increased apoptosis in lamina propria B cells during polymicrobial sepsis is FasL but not endotoxin mediated. Am. J. Physiol. Gastrointest. Liver Physiol. 280, G812-G818.
44. Hiramatsu, M., Hotchkiss, R. S., Karl, I. E., Buchman, T. G. (1997) Cecal ligation and puncture (CLP) induces apoptosis in thymus, spleen, lung, and gut by an endotoxin and TNF-independent pathway. Shock 7, 247-253.
45. Hotchkiss, R. S., Swanson, P. E., Cobb, J. P., Jacobson, A., Buchman, T. G., Karl, I. E. (1997) Apoptosis in lymphoid and parenchymal cells during sepsis: findings in normal and T- and B-cell-deficient mice. Crit. Care Med. 25, 1298-1307.
46. Docke, W. D., Randow, F., Syrbe, U., Krausch, D., Asadullah, K., Reinke, P., Volke, H. D., Kox, W. J. (1997) Monocyte deactivation in septic patients: restoration by IFN-γ treatment. Nat. Med. 3, 678-681.
47. Hotchkiss, R. S., Chang, K. C., Grayson, M. H., Tinsley, K. W., Dunne, B. S., Davis, C. G., Osborne, D. F., Karl, I. E. (2003) Adoptive transfer of apoptotic splenocytes worsens survival, whereas adoptive transfer of necrotic splenocytes improves survival in sepsis. Proc. Natl. Acad. Sci. USA 100, 6724-6729.
48. Ayala, A., Perrin, M. M., Wagner, M. A., Chaudry, I. H. (1990) Enhanced susceptibility to sepsis following simple hemorrhage: depression of Fc and C3b receptor-mediated phagocytosis. Arch. Surg. 125, 70-75.
49. Rana, M. W., Ayala, A., Dean, R. E., Chaudry, I. H. (1990) Decreased Fc receptor expression on macrophages following simple hemorrhage as observed by scanning immunoelectron microscopy. J. Leukoc. Biol. 48, 512-518.
50. Solomkin, J. S., Jenkins, M. K., Nelson, R. D., Chenoweth, D., Simmons, R. L. (1981) Neutrophil dysfunction in sepsis. II. Evidence for the role of complement activation products in cellular deactivation. Surgery 90, 319-327.
51. Huber-Lang, M., Sarma, V. J., Lu, K. T., McGuire, S. R., Padgaonkar, V. A., Guo, R. F., Younkin, E. M., Kunkel, R. G., Ding, J., Erickson, R., Curnette, J. T., Ward, P. A. (2001) Role of C5a in multiorgan failure during sepsis. J. Immunol. 166, 1193-1199.
52. Huber-Lang, M. S., Riedemann, N. C., Sarma, J. V., Younkin, E. M., McGuire, S. R., Laudes, I. J., Lu, K. T., Guo, R. F., Neff, T. A., Padgaonkar, V. A., Lambris, J. D., Spruce, L., Mastellos, D., Zetoune, F. S., Ward, P. A. (2002) Protection of innate immunity by C5aR antagonist in septic mice. FASEB J. 16, 1567-1574.
53. Vandivier, R. W., Fadok, V. A., Ogden, C. A., Hoffmann, P. R., Brain, J. D., Accurso, F. J., Fisher, J. H., Greene, K. E., Henson, P. M. (2002) Impaired clearance of apoptotic cells from cystic fibrosis airways. Chest 121, 89S.
54. Vandivier, R. W., Fadok, V. A., Hoffmann, P. R., Bratton, D. L., Penvari, C., Brown, K. K., Brain, J. D., Accurso, F. J., Henson, P. M. (2002) Elastase-mediated phosphatidylserine receptor cleavage impairs apoptotic cell clearance in cystic fibrosis and bronchiectasis. J. Clin. Invest. 109, 661-670.
55. Brazil, D. P., Hemmings, B. A. (2001) Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem. Sci. 26, 657-664.
56. Datta, S. R., Brunet, A., Greenberg, M. E. (1999) Cellular survival: a play in three Akts. Genes Dev. 13, 2905-2927.
57. Brunet, A., Bonni, A., Zigmond, M. J., Lin, M. Z., Juo, P., Hu, L. S., Anderson, A. J., Arden, K. C., Blenis, J., Greenberg, M. E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 96, 857-868.
58. Bommhardt, U., Chang, K. C., Swanson, P. E., Wagner, T. H., Tinsley, K. W., Karl, I. E., Hotchkiss, R. S. (2004) Akt decreases lymphocyte apoptosis and improves survival in sepsis. J. Immunol. 172, 7583-7591.
59. Iwata, A., Stevenson, V. M., Minard, A., Tasch, M., Tupper, J., Lagasse, E., Weissman, I., Harlan, J. M., Winn, R. K. (2003) Over-expression of Bcl-2 provides protection in septic mice by a trans effect. J. Immunol. 171, 3136-3141.
60. Javadi, P., Buchman, T. G., Stromberg, P. E., Husain, K. D., Dunne, W. M., Woolsey, C. A., Turnbull, I. R., Hotchkiss, R. S., Karl, I. E., Coopersmith, C. M. (2004) High-dose exogenous iron following cecal ligation and puncture increases mortality rate in mice and is associated with an increase in gut epithelial and splenic apoptosis. Crit. Care Med. 32, 1178-1185.
61. Doherty, C. P., Weaver, L. T., Prentice, A. M. (2002) Micronutrient supplementation and infection: a double-edged sword? J. Pediatr. Gastroenterol. Nutr. 34, 346-352.
62. Kochan, I. (1973) The role of iron in bacterial infections, with special consideration of host-tubercle bacillus interaction. Curr. Top. Microbiol. Immunol. 60, 1-30.
63. Ayala, A., Xu, Y. X., Ayala, C. A., Sonefeld, D. E., Karr, S. M., Evans, T. A., Chaudry, I. H. (1998) Increased mucosal B-lymphocyte apoptosis during polymicrobial sepsis is a Fas ligand but not an endotoxin-mediated process. Blood 91, 1362-1372.
64. Chung, C. S., Xu, Y. X., Wang, W., Chaudry, I. H., Ayala, A. (1998) Is Fas ligand or endotoxin responsible for mucosal lymphocyte apoptosis in sepsis? Arch. Surg. 133, 1213-1220.
65. Le Tulzo, Y., Pangault, C., Gacouin, A., Guilloux, V., Tribut, O., Amiot, L., Tattevin, P., Thomas, R., Fauchet, R., Drénou, B. (2002) Early circulating lymphocyle apoplosis in human seplic shock is associated with poor outcome. Shock 18, 487-494.
66. Papathanassoglou, E. D. E., Moynihan, J. A., Vermillion, D. L., McDermott, M. P., Ackerman, M. H. (2000) Soluble Fas levels correlate with multiple organ dysfunction severity, survival and nitrate levels, but not with cellular apoptotic markers in critically ill patients. Shock 14, 107-112.
67. Hotchkiss, R. S., Osmon, S. B., Chang, K. C., Wagner, T. H., Coopersmith, C. M., Karl, I. E. (2005) Accelerated lymphocyte death in sepsis occurs by both the death receptor and mitochondrial pathway. J. Immunol. 174, 5110-5118.
68. De Freitas, I., Fernandez-Somoza, M., Essenfeld-Sekler, E., Cardier, J. E. (2004) Serum levels of the apoptosis-associated molecules, tumor necrosis factor-α/tumor necrosis factor type-1 receptor and FAS/FASL in sepsis. Chest 125, 2238-2246.
69. Papathanassoglou, E. D. E., Moynihan, J. A., McDermott, M. P., Ackerman, M. H. (2001) Expression of Fas (CD95) and Fas ligand on peripheral blood mononuclear cells in critical illness and association with multiorgan dysfunction severity and survival. Crit. Care Med. 29, 709-718.
70. Roth, G., Moser, B., Krenn, C., Brunner, M., Haisjackl, M., Almer, G., Wolner, E., Boltz-Nitulescu, G., Ankersmit, H. J. (2003) Susceptibility to programmed cell death in T-lymphocytes of septic patients: a mechanism of lymphopenia and Th2 predominance. Biochem. Biophys. Res. Commun. 308, 840-846.
71. Efron, P., Moldawer, L. L. (2003) Sepsis and the dendritic cell. Shock 20, 386-401.
72. Ding, Y., Chung, C. S., Newton, S., Chen, Y., Carlton, S., Albina, J. E., Ayala, A. (2004) Polymicrobial sepsis induces divergent effects on splenic and peritoneal dendritic cell function in mice. Shock 22, 137-144.
73. Efron, P. A., Martins, A., Minnich, D., Tinsley, K. W., Ungaro, R., Bahjat, F. R., Hotchkiss, R. S., Clare-Salzler, M., Moldawer, L. L. (2004) Characterization of the systemic loss of dendritic cells in murine lymph nodes during polymicrobial sepsis. J. Immunol. 173, 3035-3043.
74. Coopersmith, C. M., Stromberg, P. E., Dunne, W. M., Davis, C. G., Amiot, I. D. M., Buchman, T. G., Karl, I. E., Hotchkiss, R. S. (2002) Inhibition of intestinal epithelial apoptosis and survival in a murine model of pneumonia-induced sepsis. JAMA 287, 1716-1721.
75. Coopersmith, C. M., Chang, K. C., Swanson, P. E., Tinsley, K. W., Stromberg, P. E., Buchman, T. G., Karl, I. E., Hotchkiss, R. S. (2002) Overexpression of Bcl-2 in the intestinal epithelium improves survival in septic mice. Crit. Care Med. 30, 195-201.
76. Hotchkiss, R., Karl, I. E. (2004) Endothelial cell apoptosis in sepsis: a case of habeas corpus? Crit. Care Med. 32, 901-902.
77. Mutunga, M., Fulton, B., Bullock, R., Batchelor, A., Gascoigne, A., Gillespie, J. I., Baudouin, S. V. (2001) Circulating endothelial cells in patients with septic shock. Am. J. Respir. Crit. Care Med. 163, 195-200.
78. Minagar, A., Jy, W., Jimenez, J. J., Sheremata, W. A., Mauro, L. M., Mao, W. W., Horstman, L. L., Ahn, Y. S. (2001) Elevated plasma endothelial microparticles in multiple sclerosis. Neurology 56, 1319-1324.
79. Zhou, M., Simms, H. H., Wang, P. (2004) Adrenomedullin and adrenomedullin binding protein-1 attenuate vascular endothelial cell apoptosis in sepsis. Ann. Surg. 240, 321-330.
80. Roth, G. A., Krenn, C., Brunner, M., Moser, B., Ploder, M., Spittler, A., Pelinka, L., Sautner, T., Wolner, E., Boltz-Nitulescu, G., Ankersmit, H. J. (2004) Elevated serum levels of epithelial cell apoptosis-specific cytokeratin 18 neoepitope m30 in critically ill patients. Shock 22, 218-220.
81. Song, G. Y., Chung, C. S., Chaudry, I. H., Ayala, A. (2000) Immune suppression in polymicrobial sepsis: differential regulation of Th1 and Th2 lymphocyte responses by p38 MAPK. J. Surg. Res. 91, 141-146.
82. Hildeman, D. A., Mitchell, T., Teague, T., Henson, P., Day, B. J., Kappler, J., Marrack, P. C. (1999) Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 10, 735-744.
83. Bernard, G. R., Artigas, A., Brigham, K. L. (1994) The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes and clinical trails coordination. Am. J. Respir. Crit. Care Med. 149, 818-824.
84. Ayala, A., Chung, C. S., Lomas, J. L., Song, G. Y., Doughty, L. A., Gregory, S. H., Cioffi, W. G., LeBlanc, B. W., Reichner, J., Simms, H. H., Grutkoski, P. S. (2002) Shock-induced neutrophil-mediated priming for acute lung injury in mice: divergent effects of TLR-4 and TLR-4/FasL deficiency. Am. J. Pathol. 161, 2283-2294.
85. Morrison, R. J., Bidani, A. (2002) Acute respiratory distress syndrome epidemiology and pathophysiology. Chest Surg. Clin. N. Am. 12, 301-323.
86. DosReis, G. A., Borges, V. M., Zin, W. A. (2004) The central role of Fas-ligand cell signaling in inflammatory lung diseases. J. Cell. Mol. Med. 8, 285-293.
87. Shimabukuro, D. W., Sawa, T., Cropper, M. A. (2003) Injury and repair in lung and airways. Crit. Care Med. 31, S524-S531.
88. Nakamura, M., Matute-Bello, G., Liles, W. C., Hayashi, S., Kajikawa, O., Lin, S-M., Frevert, C. W., Martin, T. R. (2004) Differential response of human lung epithelial cells to Fas-induced apoptosis. Am. J. Pathol. 164, 1949-1958.
89. Liles, W. C., Kiener, P. A., Ledbetter, J. A., Aruffo, A., Klebanoff, S. J. (1996) Differential expression of Fas (CD95) and Fas ligand on normal human phagocytes: implications for the regulation of apoptosis in neutrophils. J. Exp. Med. 184, 429-440.
90. Morimoto, K., Amano, H., Sonoda, F., Baba, M., Senba, M., Yoshimine, H., Yamamoto, H., Ii, T., Oishi, K., Nagatake, T. (2001) Alveolar macrophages that phagocytose apoptotic neutrophils produce hepatocyte growth factor during bacterial pneumonia in mice. Am. J. Respir. Cell Mol. Biol. 24, 608-615.
91. Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., Henson, P. M. (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/ paracrine mechanisms involving TGF-β, PGE2, and PAF. J. Clin. Invest. 101, 890-898.
92. Bardales, R. H., Xie, S. S., Schaefer, R. F., Hsu, S. M. (1996) Apoptosis is a major pathway responsible for the resolution of type II pneumocytes in acute lung injury. Am. J. Pathol. 149, 845-852.
93. Guinee Jr., D., Brambilla, E., Fleming, M., Hayashi, T., Rahn, M., Koss, M., Ferrans, V., Travis, W. (1997) The potential role of BAX and BCL-2 expression in diffuse alveolar damage. Am. J. Pathol. 151, 999-1007.
94. Hotchkiss, R. S., Dunne, W. M., Swanson, P. E., Davis, C. G., Tinsley, K. W., Chang, K. C., Buchman, T. G., Karl, I. E. (2001) Role of apoptosis in Pseudomonas aeruginosa pneumonia. Science 294, 1783.
95. Bannerman, D. D., Goldblum, S. E. (2003) Mechanisms of bacterial lipopolysaccharide-induced endothelial apoptosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 284, L899-L914.
96. Bao, S., Wang, Y., Sweeney, P., Chaudhuri, A., Doseff, A. I., Marsh, C. B., Knoell, D. L. (2005) Keratinocyte growth factor induces Akt kinase activity and inhibits Fas-mediated apoptosis in A549 lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 288, L36-L42.
97. Wickel, D. J., Cheadle, W. G., Mercer-Jones, M. A., Garrison, R. N. (1997) Poor outcome from peritonitis is caused by disease acuity and organ failure, not recurrent peritoneal infection. Ann. Surg. 225, 744-753.
98. Walley, K. R., Lukacs, N. W., Standiford, T. J., Strieter, R. M., Kunkel, S. L. (1997) Elevated levels of macrophage inflammatory protein 2 in severe murine peritonitis increase neutrophil recruitment and mortality. Infect. Immun. 65, 3847-3851.
99. Lomas, J. L., Chung, C. S., Grutkoski, P. S., LeBlanc, B. W., Lavigne, L., Reichner, J., Gregory, S. H., Doughty, L. A., Cioffi, W. G., Ayala, A. (2003) Differential effects of macrophage inflammatory protein-2 and keratinocyte-derived chemokine on hemorrhage-induced neutrophil priming for lung inflammation: assessment by adoptive cell transfer in mice. Shock 19, 358-365.
100. Parsey, M. V., Kaneko, D., Shenkar, R., Abraham, E. (1999) Neutrophil apoptosis in the lung after hemorrhage or endotoxemia: apoptosis and migration are independent of IL-1 β. Clin. Immunol. 91, 219-225.
101. Jimenez, M. F., Watson, W. G., Parodo, J., Evans, D., Foster, D., Steinberg, M., Rotstein, O. D., Marshall, J. C. (1997) Dysregulated expression of neutrophil apoptosis in the systemic inflammatory response syndrome. Arch. Surg. 132, 1263-1270.
102. Chitnis, D., Dickerson, C., Munster, A. M., Winchurch, R. A. (1996) Inhibition of apoptosis in polymorphonuclear neutrophils from burn patients. J. Leukoc. Biol. 59, 835-839.
103. Fanning, N. F., Kell, M. R., Shorten, G. D., Kirwan, W. O., Bouchier-Hayes, D., Cotter, T. G., Redmond, H. P. (1999) Circulating granulocyte macrophage colony-stimulating factor in plasma of patients with the systemic inflammatory response syndrome delays neutrophil apoptosis through inhibition of spontaneous reactive oxygen species generation. Shock 11, 167-174.
104. Ayala, A., Karr, S. M., Evans, T. A., Chaudry, I. H. (1997) Factors responsible for peritoneal granulocyte apoptosis during sepsis. J. Surg. Res. 69, 67-75.
105. Leuenroth, S. J., Grutkoski, P. S., Ayala, A., Simms, H. H. (2000) The loss of Mcl-1 expression in human polymorphonuclear leukocytes promotes apoptosis. J. Leukoc. Biol. 68, 158-166.
106. Dibbert, B., Weber, M., Nikolaizik, W. H., Vogt, P., Schöni, M. H., Blaser, K., Simon, H-U. (1999) Cytokine-mediated Box deficiency and consequent delayed neutrophil apoptosis: a general mechanism to accumulate effector cells in inflammation. Proc. Natl. Acad. Sci. USA 96, 13330-13335.
107. Moulding, D. A., Akgul, C., Derouet, M., White, M. R. H., Edwards, S. W. (2001) Bcl-2 family expression in human neutrophils during delayed and accelerated apoptosis. J. Leukoc. Biol. 70, 783-792.
108. Moulding, D. A., Quayle, J. A., Hart, C. A., Edwards, S. W. (1998) Mcl-1 expression in human neutrophils: regulation by cytokines and correlation with cell survival. Blood 92, 2495-2502.
109. Chuang, P. I., Yee, E., Karsan, A., Winn, R. K., Harlan, J. M. (1998) A1 is a constitutive and inducible Bcl-2 homologue in mature human neutrophils. Biochem. Biophys. Res. Commun. 249, 361-365.
110. Villunger, A., O'Reilly, L. A., Holler, N., Adams, J., Strasser, A. (2000) Fas ligand, Bcl-2, granulocyte colony-stimulating factor, and p38 mitogen-activated protein kinase: regulators of distinct cell death and survival pathways in granulocytes. J. Exp. Med. 192, 647-657.
111. L- and Bax-α-mediated regulation of apoptosis of human neutrophils via capase-3. Blood 93, 3106-3115.
112. Weaver, J. G. R., Rouse, M. R., Steckelburg, J. M., Badley, A. M. (2004) Improved survival in experimental sepsis with an orally administered inhibitor of apoptosis. FASEB J. 18, 1185-1191.
113. Sookhai, S., Wang, J. J., McCourt, M., Kirwan, W., Bouchier-Hayes, D., Redmond, P. (2002) A novel therapeutic strategy for attenuating neutrophil-mediated lung injury in vivo. Ann. Surg. 235, 285-291.
114. Huynh, M. L., Fadok, V. A., Henson, P. M. (2002) Phosphatidylserine- dependent ingestion of apoptotic cells promotes TGF-β 1 secretion and the resolution of inflammation. J. Clin. Invest. 109, 41-50.
115. Genestier, L., Kasibhatla, S., Brunner, T., Green, D. R. (1999) Transforming growth factor β1 inhibits Fas ligand expression and subsequent activation-induced cell death in T cells via downregulation of c-Myc. J. Exp. Med. 189, 231-239.
116. Lu, M-C., Liu, T-A., Lee, M-R., Lin, L., Chang, W-C. (2002) Apoptosis contributes to the decrement in numbers of alveolar macrophages from rats with polymicrobial sepsis. J. Microbiol. Immunol. Infect. 35, 71-77.
117. Ayala, A., Urbanich, M. A., Herdon, C. D., Chaudry, I. H. (1996) Is sepsis-induced apoptosis associated with macrophage dysfunction? J. Trauma 40, 568-574.
118. Williams, T. E., Ayala, A., Chaudry, I. H. (1997) Inducible macrophage apoptosis following sepsis is mediated by cysteine protease activation and nitric oxide release. J. Surg. Res. 70, 113-118.
119. Williams, M. A., Withington, S., Newland, A. C., Kelsey, S. M. (1998) Monocyte anergy in septic shock is associated with a predilection to apoptosis and is reversed by granulocyte-macrophage colony stimulating factor ex vivo. J. Infect. Dis. 178, 1421-1433.
120. Kitamura, Y., Hashimoto, S., Mizuta, N., Kobayashi, A., Kunihiko, K., Fujiwara, I., Nakajima, H. (2001) Fas/FasL-dependent apoptosis of alveolar cells after lipopolysaccharide-induced lung injury in mice. Am. J. Respir. Crit. Care Med. 163, 762-769.
121. Vernooy, J. H., Dentener, M. A., van Suylen, R. J., Buurman, W. A., Wouters, E. F. (2001) Intratracheal instillation of lipopolysaccharide in mice induces apoptosis in bronchial epithelial cells: no role for tumor necrosis factor-α and infiltrating neutrophils. Am. J. Respir. Cell Mol. Biol. 24, 569-576.
122. Serrao, K. L., Fortenberry, J. D., Owens, M. L., Harris, F. L., Brown, L. A. (2001) Neutrophils induce apoptosis of lung epithelial cells via release of soluble Fas ligand. Am. J. Physiol. Lung Cell. Mol. Physiol. 280, L298-L305.
123. Albertine, K. H., Soulier, M. F., Wang, Z., Ishizaka, A., Hashimoto, S., Zimmerman, G. A., Matthay, M. A., Ware, L. B. (2002) Fas and Fas ligand are up-regulated in pulmonary edema fluid and lung tissue of patients with acute lung injury and the acute respiratory distress syndrome. Am. J. Pathol. 161, 1783-1796.
124. Guinee Jr., D., Brambilla, E., Fleming, M., Hayashi, T., Rahn, M., Koss, M., Ferrans, V., Travis, W. (1997) The potential role of BAX and BCL-2 expression in diffuse alveolar damage. Am. J. Pathol. 151, 999-1007.
125. Matute-Bello, G., Winn, R. K., Jonas, M., Chi, E. Y., Martin, T. R., Liles, W. C. (2001) Fas (CD95) induces alveolar epithelial cell apoptosis in vivo. Am. J. Pathol. 158, 153-161.
126. Meyrick, B. O. (1986) Endotoxin-mediated pulmonary endothelial cell injury. Fed. Proc. 45, 19-24.
127. Hotchkiss, R. S., Karl, I. E. (2004) Endothelial cell apoptosis in sepsis: a case of habeas corpus? Crit. Care Med. 32, 901-902.
128. Pohlman, T. H., Harlan, J. M. (1989) Human endothelial cell response to lipopolysaccharide, interleukin-1, and tumor necrosis factor is regulated by protein synthesis. Cell. Immunol. 119, 41-52.
129. Hu, X., Yee, E., Harlan, J. M., Wong, F., Karsan, A. (1998) Lipopolysaccharide induces the antiapoptotic molecules, A1 and A20, in microvascular endothelial cells. Blood 92, 2759-2765.
130. Haimovitz-Friedman, A., Cordon-Cardo, C., Bayoumy, S., Garzotto, M., McLoughlin, M., Gallily, R., Edwards, C. K., Schuchman, E. H., Fuks, Z., Kolesnick, R. (1997) Lipopolysaccharide induces disseminated endothelial apoptosis requiring ceramide generation. J. Exp. Med. 186, 1831-1841.
131. Fujita, M., Kuwano, K., Kunitake, R., Hagimoto, N., Miyazaki, H., Kaneko, Y., Kawasaki, M., Maeyama, T., Hara, N. (1998) Endothelial cell apoptosis in lipopolysaccharide-induced lung injury in mice. Int. Arch. Allergy Immunol. 117, 202-208.
132. Kawasaki, M., Kuwano, K., Hagimoto, N., Matsuba, T., Kunitake, R., Tanaka, T., Maeyama, T., Hara, N. (2000) Protection from lethal apoptosis in lipopolysaccharide-induced acute lung injury in mice by a caspase inhibitor. Am. J. Pathol. 157, 597-603.
133. Lu, Q., Xu, D-Z., Davidson, M. T., Hasko, G., Deitch, E. A. (2004) Hemorrhagic shock induces endothelial cell apoptosis, which is mediated by factors contained in mesenteric lymph. Crit. Care Med. 32, 2464-2470.
134. Beck, J. M., Preston, A. M., Wilcoxen, S. E., Morris, S. B., White, E. S., Paine III, R. (2003) Pneumocystis pneumonia increases the susceptibility of mice to sublethal hyperoxia. Infect. Immun. 71, 5970-5978.
135. Hao, Z., Hampel, B., Yagita, H., Rajewsky, K. (2004) T cell-specific ablation of Fas leads to Fas ligand-mediated lymphocyte depletion and inflammatory pulmonary fibrosis. J. Exp. Med. 199, 1355-1365.
136. Lenardo, M., Chan, F. K. M., Hornung, F., McFarland, H., Siegel, R., Wang, J., Zheng, L. (1999) Mature lymphocyte apoptosis-immune regulation in a dynamic and unpredictable antigenic environment. Annu. Rev. Immunol. 17, 221-253.
137. Xu, Y. X., Ayala, A., Monfils, B., Cioffi, W. G., Chaudry, I. H. (1997) Mechanism of intestinal mucosal immune dysfunction following trauma-hemorrhage: increased apoptosis associated with elevated Fas expression in Peyer's Patches. J. Surg. Res. 70, 55-60.
138. Hotchkiss, R. S., Schmieg Jr., R. E., Swanson, P. E., Freeman, B. D., Tinsley, K. W., Cobb, J. P., Karl, I. E., Buchman, T. G. (2000) Rapid onset of intestinal epithelial and lymphocyte apoptotic cell death in patients with trauma and shock. Crit. Care Med. 28, 3207-3217.
139. Xu, Y. X., Wichmann, M. W., Ayala, A., Cioffi, W. G., Chaudry, I. H. (1997) Trauma-hemorrhage induces thymic apoptosis while decreasing IL-3 release and increasing GM-CSF. J. Surg. Res. 68, 24-30.
140. Middleton, G., Reid, L. E., Harmon, B. V. (1994) Apoptosis in the human thymus in sudden and delayed death. Pathology 26, 81-89.
141. Teodorczyk-Injeyan, J. A., Cembrzynska-Nowak, M., Lalani, S., Peters, W. J., Mills, G. B. (1995) Immune deficiency following thermal trauma is associated with apoptotic cell death. J. Clin. Immunol. 15, 318-328.
142. Oka, M., Hirazawa, K., Yamamoto, K., Iizuka, N., Hazama, S., Suzuki, T., Kobayashi, N. (1996) Induction of Fas-mediated apoptosis on circulating lymphocytes by surgical stress. Ann. Surg. 223, 434-440.
143. Schroeder, S., Lindemann, C., Decker, D., Klaschik, S., Hering, R., Putensen, C., Hoeft, A., von Ruecker, A., Stüber, F. (2001) Increased susceptibility to apoptosis in circulating lymphocytes of critically ill patients. Langenbecks Arch. Surg. 386, 42-46.
144. Pellegrini, J. D., De, A. K., Kodys, K., Puyana, J. C., Furse, R. K., Miller-Graziano, C. (2000) Relationships between T lymphocyte apoptosis and anergy following trauma. J. Surg. Res. 88, 200-206.
145. Delogu, G., Famularo, G., Moretti, S., De Luca, A., Tellan, G., Antonucci, A., Marandola, M., Signore, L. (2001) Interleukin-10 and apoptotic death of circulating lymphocytes in surgical/anesthesia trauma. J. Trauma 51, 92-97.
146. Schwacha, M. G., Ayala, A., Chaudry, I. H. (2000) Insights into the role of γδ lymphocytes in the immunopathogenic response to thermal injury. J. Leukoc. Biol. 67, 644-650.
147. Venet, F., Pachot, A., Debard, A. L., Bohe, J., Bienvenu, J., Lepape, A., Monneret, G. (2004) Increased percentage of CD4+CD25+ regulatory T cells during septic shock is due to the decrease of CD4+CD25- lymphocytes. Crit. Care Med. 32, 2329-2331.
148. Rhee, R. J., Carlton, S., Lomas, J. L., Lane, C., Brossay, L., Ayala, A. (2003) Inhibition of CD1d activation suppresses septic mortality: a role for NK-T cells in septic immune dysfunction. J. Surg. Res. 115, 74-81.
149. Faunce, D. E., Gamelli, R. L., Choudry, M. A., Kovacs, E. J. (2003) A role for CD1d-restricted NKT cells in injury-associated T cell suppression. J. Leukoc. Biol. 73, 747-755.
150. Smyth, M. J., Cretney, E., Wiltrout, R. H., Sedger, L. M., Kayagaki, N., Yagita, H., Okumura, K. (2001) Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) contributes to interferon γ-dependent natural killer cell protection from tumor metastasis. J. Exp. Med. 193, 661-670.
151. van der Vliet, H. J., von Bloomberg, B. M., Hazenberg, M. D., Nishi, N., Otto, S. A., van Benthem, B. H., Prins, M., Claessen, F. A., van den Eertwegh, A. J., Giaccone, G., Miedema, F., Scheper, R. J., Pinedo, H. M. (2002) Selective decrease in circulating V α 24 + V β 11 + NKT cells during HIV type 1 infection. J. Immunol. 168, 1490-1495.
152. Hobbs, J. A., Cho, S., Roberts, T. J., Sriram, V., Zhang, J., Xu, M., Brutkiewicz, R. R. (2001) Selective loss of natural killer T cells by apoptosis following infection with lymphocytic choriomeningitis virus. J. Virol. 75, 10746-10754.
153. Chen, X., Murakami, T., Oppenheim, J. J. (2004) Differential response of murine CD4+CD25+ and CD4+CD25- T cells to dexamethasone-induced cell death. Eur. J. Immunol. 34, 859-869.
154. Banz, A., Pontoux, C., Papiernik, M. (2002) Modulation of Fas-dependent apoptosis: a dynamic process controlling both the persistence and death of regulatory T cells and effector T cells. J. Immunol. 169, 750-757.
155. Wesche, D. E., Chung, C. S., Lomas-Neira, J., Gregory, S. H., Ayala, A.
156. Hotchkiss, R. S., Chang, K. C., Swanson, P. E., Tinsley, K. W., Hui, J. J., Klender, P., Xanthoudakis, S., Roy, S., Black, C., Grimm, E., Aspiotis, R., Han, Y., Nicholson, D. W., Karl, I. E. (2000) Caspase inhibitors improve survival in sepsis: a critical role of the lymphocyte. Nat. Immunol. 1, 496-501.
157. Hotchkiss, R. S., Tinsley, K. W., Hui, J. J., Chang, K. C., Swanson, P. E., Drewry, A. M., Buchman, T. G., Karl, I. E. (2000) p53-dependent and -independent pathways of apoptotic cell death in sepsis. J. Immunol. 164, 3675-3680.
158. Yang, S., Zhou, M., Chaudry, I. H., Wang, P. (2002) Novel approach to prevent the transition from the hyperdynamic phase to the hypodynamic phase of sepsis; role of adrenomedullin and adrenomedullin binding protein-1. Ann. Surg. 236, 625-633.
159. Schotte, P., Declercq, W., Van Huffel, S., Vandenabeele, P., Beyaert, R. (1999) Non-specific effects of methyl ketone peptide inhibitors of caspases. FEBS Lett. 442, 117-121.
160. Caserta, T. M., Smith, A. N., Gultice, A. D., Reedy, M. A., Brown, T. L. (2003) Q-VD-OPh, a broad spectrum caspase inhibitor with potent antiapoptotic properties. Apoptosis 8, 345-352.
161. Wesche, D. E., Chung, C. S., Lomas-Neira, J., Gregory, S. H., Ayala, A. (2004) 'Hydrodrynamic' administration of Fas siRNA prevents liver damage and improves survival of septic mice. FASEB J. 19, 1479.
162. Wang, P., Chaudry, I. H. (1996) Mechanism of hepatocellular dysfunction during hyperdynamic sepsis. Am. J. Physiol. 270, R927-R938.
163. Chaudry, I. H., Schleck, S., Clemens, M. G., Kupper, T. E., Baue, A. E. (1982) Altered hepatocellular active transport. An early change in peritonitis. Arch. Surg. 117, 151-157.
164. Song, E., Lee, S-K., Wang, J., Ince, N., Ouyang, N., Min, J., Chen, J., Shankar, P., Lieberman, J. (2003) RNA interference targeting Fas protects mice from fulminant hepatitis. Nat. Med. 9, 347-351.