Does programmed cell death (apoptosis) play a role in the development of multiple organ dysfunction in critically ill patients? A review and a theoretical framework

Critical Care Medicine

Volumn 28, Issue 2, 2000, Pages 537-549

  Papathanassoglou, Elizabeth D E ^b   Moynihan, Jan A ^a   Ackerman, Michael H ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Cytokines; Glucocorticoids; Heat shock proteins; Interleukin 6; Interleukin 1; Interleukin 10; Multiple organ dysfunction syndrome; Nitric oxide; Oxygen free radicals; Programmed cell death; Prostaglandins; Systemic inflammatory response syndrome; Tumor necrosis factor

Indexed keywords

CYTOKINE; FREE RADICAL; GAMMA INTERFERON; GLUCOCORTICOID; HEAT SHOCK PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; NITRIC OXIDE; PROSTAGLANDIN; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

ADULT RESPIRATORY DISTRESS SYNDROME; ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DEATH; CLINICAL ARTICLE; CONTROLLED STUDY; CRITICAL ILLNESS; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; INFLAMMATION; MULTIPLE ORGAN FAILURE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL;

EID: 0034101765     PISSN: 00903493     EISSN: None     Source Type: Journal    
DOI: 10.1097/00003246-200002000-00042     Document Type: Article

References (116)

1. 1. Darville T, Giroir B, Jacobs R: The systemic inflammatory response syndrome (SIRS): Immunology and potential immunotherapy. Infection 1993; 21:279-290
2. 2. Knaus WA, Draper EA, Wagner DP, et al: Prognosis in acute organ-system failure. Ann Surg 1985; 202:685-693
3. 3. Barriere SL, Lowry SF: An overview of mortality risk prediction in sepsis. Crit Care Med 1995; 23:276-393
4. 4. Marshall JC, Cook DJ, Christou NV, et al: Multiple Organ Dysfunction Score: A reliable descriptor of a complex clinical outcome. Crit Care Med 1995; 23:1638-1652
5. 5. Bone RC: Toward a theory regarding the pathogenesis of the systemic inflammatory response syndrome: What we do and do not know about cytokine regulation. Crit Care Med 1996; 24:163-172
6. 6. Darzynkiewicz Z, Juan G, Li X, et al: Cytometry in cell necrobiology: Analysis of apoptosis and accidental cell death (necrosis). Cytometry 1997; 27:1-20
7. 7. Itoh N, Nagata S: A novel protein domain required for apoptosis. J Biol Chem 1993; 268:10932-10937
8. 8. Wallach D: Suicide by order: Some open questions about the cell-killing activities of the TNF ligand and receptor families. Cytokine Growth Factor Rev 1996; 7:211-221
9. 9. Boldin MP, Goncharov TM, Goltsev YV, et al: Involvement of MACH, a novel MORT1/ FADD-interacting protease in Fas/APO-1 and TNF receptor-induced cell death. Cell 1996; 85:803-815
10. 10. Miller DK: The role of Caspase family of cysteine proteases in apoptosis. Semin Immunol 1997; 9:35-49
11. 11. Yuan J: Transducing signals of life and death. Curr Opin Cell Biol 1997; 9:247-251
12. 12. Chinnaiyan AM, Dixit VM: Portrait of an executioner: The molecular mechanism of Fas/APO-1 induced apoptosis. Semin Immunol 1997; 9:69-75
13. 13. Cheng J, Zhou T, Liu C, et al: Protection from fas-mediated apoptosis by a soluble form of the fas molecule. Science 1994; 263:1759-1762
14. 14. Owen-Schaub LB, Angelo LS, Radinsky R, et al: Soluble Fas/APO-1 in tumor cells: a potential regulator of apoptosis? Cancer Lett 1995; 94:1-8
15. 15. Cascino I, Fiucci G, Papoff G, et al: Three functional soluble forms of the human apoptosis-inducing fas molecule are produced by alternative splicing. J Immunol 1995; 154:2706-2713
16. 16. Tanaka M, Suda T, Takahashi T, et al: Expression of the functional soluble form of human fas ligand in activated lymphocytes. EMBO J 1995; 14:1129-1135
17. 17. Liles WC, Kiener PA, Ledbetter JA, et al: Differential expression of fas (CD95) and fas ligand on normal human phagocytes: Implications for the regulation of apoptosis in neutrophils. J Exp Med 1996; 184:429-440
18. 18. Oyaizu N, Adachi Y, Hashimoto F, et al: Monocytes express fas ligand upon CD4 cross-linking and induce CD4+ T cell apoptosis. J Immunol 1997; 158:2456-2463
19. 19. Kerr JFR, Harmon BV: Definition and incidence of apoptosis: An historical perspective. Curr Commun Cell Mol Biol 1991; 3:1-27
20. 20. Buchman TG, Abello PA, Smith EH, et al: Induction of heat shock response leads to apoptosis in endothelial cells previously exposed to endotoxin. Am J Physiol 1992; 265:H165-H170
21. 21. Abello PA, Buchman TG: Heat shock-induced cell death in murine microvascular endothelial cells depends on priming with tumor necrosis factor-alpha or interferon-gamma. Shock 1994; 2:320-323
22. 22. Abello PA, Fidler SA, Bulkley GB, et al: Antioxidants modulate induction of programmed cell death (apoptosis) by endotoxin. Arch Surg 1994; 129:134-141
23. 23. Abello PA, Fidler SA, Buchman TG: Thiol reducing agents modulate induced apoptosis in porcine endothelial cells. Shock 1994; 2:79-83
24. 24. Dustin ML, Rothlein R, Bhan AK, et al: Induction of IL-1 and interferon, tissue distribution, biochemistry and function of a natural adherence molecule (ICAM-1). J Immunol 1986; 137:245-254
25. 25. McMillen MA, Huribal M, Sumpio B: Common pathway of endothelial-leukocyte interaction in shock, ischemia, and reperfusion. Am J Surg 1993; 166:557-562
26. 26. Entman ML, Youker K: Shapell SB et al: Neutrophil adherence to isolated adult canine myocytes: Evidence for a CD18-dependent mechanism. J Clin Invest 1990; 85:1497-1506
27. 27. Horgan MJ, Wright SD, Malik AB: Antibody against leukocyte integrin CD18 prevents reperfusion-induced lung vascular injury. Am J Physiol 1990; 259:315-319
28. 28. Kirton OC, Gore RG, Reid LM, et al: Recurrent episodes of gram-negative bacteremia or endotoxemia change reactivity of pre-and post-capillary pulmonary segments to angiotensin or free radicals. Intensive Care Med 1992; 18:293-298
29. 29. Ackerman MH: The systemic inflammatory response, sepsis, and multiple organ dysfunction: New definitions for an old problem. Crit Care Nurs Clin North Am 1994; 6:243-250
30. 30. Cabin DE, Buchman TG: Molecular biology of circulatory shock. Part III. Human hepatoblastoma (Hep G2) cells demonstrate two patterns of shock-induced gene expression that are independent, exclusive and prioritized. Surgery 1990; 108:902-912
31. 31. DeMeester SL, Qiu Y, Buchman TG, et al: Nitric oxide inhibits stress-induced endothelial cell apoptosis. Crit Care Med 1998; 26:1500-1509
32. 32. Tzeng E, Kim YM, Pitt BR, et al: Adenoviral transfer of the inducible nitric oxide synthase gene blocks endothelial cell apoptosis. Surgery 1997; 122:255-263
33. 33. Savill J, Hogg N, Ren Y, et al: Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J Clin Invest 1992; 90:1513-1522
34. 34. Lee A, Whyte MKB, Haslett C: Inhibition of apoptosis and prolongation of neutrophil functional longevity by inflammatory mediators. J Leukoc Biol 1990; 54:283-288
35. 35. Gadek JE: Adverse effects of neutrophils on the lung. Am J Med 1992; 92:28S-31S
36. 36. Watson RWG, Redmond HP, Wang JH, et al: Bacterial ingestion, tumor necrosis factor-alpha, and heat induce programmed cell death in activated neutrophils. Shock 1996; 5:47-51
37. 37. Ertel W, Keel M, Ungethum U, et al: Pro-inflammatory cytokines regulate apoptosis of granulocytes during systemic inflammation. Abstr. Langenbecks Arch Chir Suppl Kongressbd 1997; 114:627-629
38. 38. Wang SD, Huang KJ, Lin YS, et al: Sepsis-induced apoptosis of the thymocytes in mice. J Immunol 1994; 152:5014-5021
39. 39. Barke RA, Roy S, Chapin RB, et al: The role of programmed cell death (apoptosis) in thymic involution following sepsis. Arch Surg 1994; 129:1256-1262
40. 40. Teodorczyk-Injeyan JA, Sparkes BG, Lalani S, et al: IL-2 regulation of soluble IL-2 receptor levels following thermal injury. Clin Exp Immunol 1992; 90:36-42
41. 41. Ayala A, Herdon CD, Lehman DL, et al: Differential induction of apoptosis in lymphoid tissues during sepsis: Variation of onset, frequency, and the nature of the mediators. Blood 1996; 87:4261-4275
42. 42. Hotchkiss RS, Swanson PE, Cobb PJ, et al: Apoptosis in lymphoid and parenchymal cells during sepsis: Findings in normal and T-and B-deficient mice. Crit Care Med 1997; 25:1298-1307
43. 43. Hiramatsu M, Hotchkiss RS, Karl IE, et al: Cecal ligation and puncture (CLP) induces apoptosis in thymus, spleen, lung and gut by an endotoxin and TNF-independent pathway. Shock 1996; 7:247-253
44. 44. Maeda K, Abello PA, Abraham MR, et al: Endotoxin induces organ-specific endothelial cell injury. Shock 1995; 3:46-50
45. 45. Abello PA, Buchman TG, Bulkley GB, et al: Shock and multiple organ failure. Adv Exp Med Biol 1994; 366:253-268
46. 46. Schumer M, Colombel MC, Sawczuk IS, et al: Morphologic, biochemical, and molecular evidence of apoptosis during the reperfusion phase after brief periods of renal ischemia. Am J Pathol 1992; 140:831-838
47. 47. Polunovsky VA, Chen B, Henke C, et al: Role of mesenchymal cell death in lung remodeling after injury. J Clin Invest 1993; 92: 388-397
48. 48. Leist M, Gantner F, Bohlinger I, et al: Tumor necrosis factor-induced hepatocyte apoptosis precedes liver failure in experimental murine shock models. Am J Pathol 1995; 146:1220-1234
49. 49. Wang JH, Redmond HP, Watson RWG, et al: Role of lipopolysaccharide and tumor necrosis factor-alpha in induction of hepatocyte necrosis. Am J Physiol 1995; 269: G297-G304
50. 50. Gottlieb RA, Burleson KO, Kloner RA, et al: Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 1994; 94:1621-1628
51. 51. Kajstura J, Cheng W, Reiss K, et al: Apoptotic and necrotic myocyte cell deaths are independent contributing variables of infarct size in rats. Lab Invest 1996; 74: 86-107
52. 52. Olivetti G, Abbi R, Quaini F, et al: Apoptosis in the failing human heart. W Engl J Med 1997; 336:1131-1141
53. 53. Endo S, Inada K, Takakuwa T, et al: Nitrite/ Nitrate (NOx) and sFas antigen levels in patients with multiple organ failure. Res Commun Mol Pathol Pharmacol 1996; 92: 253-256
54. 54. Yamada Y, Endo S, Kasai T, et al: Nuclear matrix protein, tumor necrosis factor-α, and nitrite/nitrate levels in patients with multiple organ dysfunction syndrome. Res Commun Mol Pathol Pharmacol 1998; 100: 92-104
55. 55. Oka M, Hirazawa K, Yamamoto K, et al: Induction of fas-mediated apoptosis on circulating lymphocytes by surgical stress. Ann Surg 1996; 223:434-440
56. 56. Ungethum U, Keel M, Trentz O, et al: Increased expression of apoptosis-inducing proteins Fas antigen and Fas ligand on mononuclear cells of septic patients. Abstr. Langenbecks Arch Chir Suppl Kongressbd 1997; 114:623-625
57. 57. Coutinho HB, Robalinho TI, Coutinho VB, et al: Intra-abdominal sepsis: An immunocytochemical study of the small intestine mucosa. J Clin Pathol 1997; 50:294-298
58. 58. Ayala A, Karr SM, Evans TA, et al: Factors responsible for peritoneal granulocyte apoptosis during sepsis. J Surg Res 1997; 69: 67-75
59. 59. Williams TE, Ayala A, Chaudry IH: Inducible macrophage apoptosis following sepsis is mediated by cysteine protease activation and nitric oxide release. J Surg Res 1997; 70:113-118
60. 60. Bone RC: Why sepsis trials fail. JAMA 1996; 21:565-566
61. 61. Calandra T, Gerain J, Heumann D, et al: High circulating levels of interleukin-6 in patients with septic shock: Evolution during sepsis, prognostic value, and interplay with other cytokines. Am J Med 1991; 91: 23-29
62. 62. van der Poll T, Lowry SF: Tumor necrosis factor in sepsis: Mediator of multiple organ failure or essential part of host defense? Shock 1995; 3:1-12
63. 63. Baker S, Reddy P: Transducers of life and death: TNF receptor superfamily and associated proteins. Oncogene 1996; 12:1-9
64. 64. Selleri C, Sato T, Anderson S, et al: Interferon-gamma and tumor necrosis factor-alpha suppress both early and late stages of hematopoiesis and induce programmed cell death. J Cell Phys 1995; 165:538-546
65. 65. Sarih M, Souvannavong V, Adam A: Nitric oxide synthase induces macrophage death by apoptosis. Biochem Biophys Res Commun 1993; 191:503-508
66. 66. Tilg H, Dinarello CA, Mier JW: IL-6 and APPs: Anti-inflammatory and immunosuppressive mediators. Immunol Today 1997; 18:428-432
67. 67. Christman JW, Holden EP, Blackwell TS: Strategies for blocking the systemic effects of cytokines in the sepsis syndrome. Crit Care Med 1995; 23:955-963
68. 68. Afford SC, Pongracz J, Stockley RA, et al: The induction by human interleukin-6 of apoptosis in the promonocytic cell line U937 and human neutrophils. J Biol Chem 1992; 267:21612-21616
69. 69. Border EC, Chin P: Intelreukin-6: A cytokine with potential diagnostic and therapeutic roles. J Lab Clin Med 1994; 123: 824-829
70. 70. Damas P, Ledoux D, Nys M, et al: Cytokine serum levels during severe sepsis in humans: IL-6 as a marker of severity. Ann Surg 1992; 215:356-362
71. 71. Fugger R, Zadrobilek E, Gotzinger P, et al: Perioperative TNF-α and IL-6 concentrations correlate with septic state, organ function, and APACHE II scores in intraabdominal infection. Eur J Surg 1993; 159: 525-529
72. 72. Preiser JC, Schmartz D, Van der Linden P, et al: Interleukin-6 administration has no acute hemodynamic or hématologie effect in the dog. Cytokine 1991; 3:1-4
73. 73. Jirik FR, Podor TJ, Hirano T, et al: Bacterial lipopolysaccharide and inflammatory mediators augment IL-6 secretion by human endothelial cells. J Immunol 1991; 142: 144-147
74. 74. Biffl WL, Moore EE, Moore FA, et al: Interleukin-6 delays neutrophil apoptosis. Arch Surg 1996; 131:24-30
75. 75. Biffl WL, Moore EE, Moore FA, et al: Interleukin-6 delays neutrophil apoptosis via a mechanism involving platelet-activating factor. J Trauma 1996; 40:575-579
76. 76. Pruitt JH, Copeland, EM III, Moldawer LL: Interleukin-1 and interleukin-1 antagonism in sepsis, systemic inflammatory response syndrome, and septic shock. Shock 1995; 3:235-251
77. 77. Cannon JG, Friedberg JS, Gelfand JA, et al: Circulating interleukin-1 beta and tumor necrosis factor-alpha concentrations after burn injury in humans. Crit Care Med 1992; 20:1414-1419
78. 78. Mills CD, Caldwell MD, Gann DS: Evidence of a plasma-mediated "window" of immunodeficiency in rats following trauma. J Clin Immunol 1989; 9:139-150
79. 79. Ancarcrona M, Dypbukt JM., Brune B, et al: Interleukin-1 beta-induced nitric oxide production activates apoptosis in pancreatic RINm5F cells. Exp Cell Res 1994; 213: 172-177
80. 80. Kaneto H, Fujii J, Seo HG, et al: Apoptotic cell death triggered by nitric oxide in pancreatic beta-cells. Diabetes 1995; 44: 733-738
81. 81. Blanco FJ, Ochs RL, Schwarz H, et al: Chondrocyte apoptosis induced by nitric oxide. Am J Pathol 1995; 146:75-85
82. 82. Furukawa Y, Kikuchi J, Terui Y, et al: Preferential production of interleukin-1 beta over interleukin-1 receptor antagonist contributes to proliferation and suppression of apoptosis in leukemic cells. Jpn J Cancer Res 1995; 86:208-216
83. 83. Colotta F, Re F, Polentarutti N: Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 1992; 80:2012-2020
84. 84. Nalin CM: Apoptosis research enters the ICE age. Structure 1995; 3:143-145
85. 85. Ayala A, Chaudry IH: Immune dysfunction in murine polymicrobial sepsis: mediators, macrophages, lymphocytes and apoptosis. Shock 1996; 6(Suppl 1):S27-S38
86. 86. Friedman G, Jankowski S, Marchant: A et al: Blood interleukin 10 levels parallel the severity of septic shock. J Crit Care 1997; 12:183-187
87. 87. Kasai T, Inada K, Takawura T, et al: Anti-inflammatory cytokine levels in patients with septic shock. Res Commun Mol Pathol Pharmacol 1997; 98:34-42
88. 88. Neidhardt R, Keel M, Steckholzer U, et al: Relationship of interleukin-10 plasma levels to severity of injury and clinical outcome in injured patients. J Trauma 1997; 42: 863-870
89. 89. Keel M, Ungethum U, Steckholzer U, et al: Interleukin-10 counterregulates proinflammatory cytokine-induced inhibition of neutrophil apoptosis during severe sepsis. Blood 1997; 90:3356-3363
90. 90. Cox G: IL-10 enhances resolution of pulmonary inflammation in vivo by promoting apoptosis of neutrophils. Am J Physiol 1996; 271:L566-571
91. 91. Nathan C: Nitric oxide as a secretory product of mammalian cells. FASEB J 1992; 6:3051-3064
92. 92. Ochoa JB, Udekwu AO, Billiar TR, et al: Nitrogen oxide levels in patients after trauma and during sepsis. Ann Surg 1991; 214:621-626
93. 93. Stoclet J-C, Fleming I, Gray G, et al: Nitric oxide and endotoxemia. Circulation 1993; 87:V77-V80
94. 94. Fehsel K, Kronke K-D, Meyer KL, et al: Nitric oxide induces apoptosis in mouse thymocytes. J Immunol 1995; 155: 2858-2865
95. 95. Larrick JW, Wright SC: Cytotoxic mechanism of tumor necrosis factor-α. FASEB J 1990; 4:3215-3223
96. 96. Wood KA, Youle RJ: Apoptosis and free radicals. Ann N Y Acad Sci 1994; 738:400-407
97. 97. Curtis WE, Schoeniger LO, Beck SC, et al: Myocellular gene expression in response to ischemic-reperfusion injury during cardiopulmonary bypass. Surg Forum 1992; 43: 215-217
98. 98. Jaattela M, Wissing D: Emerging role of heat shock proteins in biology and medicine. Ann Med 1992; 24:249-258
99. 99. Westwood JT, Clos J Wu C: Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature 1991; 353:822-827
100. 100. Schiaffonati L, Rappocciolo E, Tacchini L, et al: Reprogramming of gene expression in postischemic rat liver: Induction of protooncogenes and hsp 70 gene family. J Cell Physiol 1990; 143:79-87
101. 101. Schoeniger LO, Reilly PM, Bulkley GB, et al: Heat-shock gene expression excludes hepatic acute-phase gene expression after resuscitation from hemorrhagic shock. Surgery 1992; 112:355-363
102. 102. Migliorati G, Nicoletti I, Crocicchio F, et al: Heat shock induces apoptosis in mouse thymocytes and protects from glucocorticoid-induced cell death. Cell Immunol 1992; 143:348-356
103. 103. Wang JH, Redmond HP, Watson RW, et al: Induction of heat shock protein 72 prevents neutrophil-mediated human endothelial cell necrosis. Arch Surg 1995; 130: 1260-1265
104. 104. Maihlos C, Hoaward MK, Latchman DS: Heat shock protects neuronal cells from programmed cell death by apoptosis. Neuroscience 1993; 55:621-627
105. 105. Smith CA, Grimes EA, McCarthy NJ, et al: Multiple gene regulation of apoptosis: Significance in immunology and oncology. Curr Commun Cell Mol Biol 1994; 8:43-88
106. 106. Perrin-Wolff M, Bertoglio J, Bressac B, et al: Structure-activity relationships in glucocorticoid-induced apoptosis in T-lymphocytes. Biochem Pharmacol 1994; 50: 1103-1110
107. 107. Schwartzman RA, Cidlowski JA: Glucocorticoid-induced apoptosis of lymphoid cells. Int Arch Allergy Immunol 1994; 105: 347-354
108. 108. King LB, Vacchio MS, Dixon K, et al: A targeted glucocorticoid receptor antisense transgene increases thymocyte apoptosis and alters thymocyte development. Immunity 1995; 3:647-656
109. 109. Migliorati G, Pagliacci C, Moraca R, et al: Interleukins modulate glucocorticoid-induced thymocyte apoptosis. Int J Clin Lab Res 1992; 21:300-303
110. 110. Cox G: Glucocorticoid treatment inhibits apoptosis in human neutrophils: Separation of survival and activation outcomes. J Immunol 1995; 154:4719-4725
111. 111. Liles WC, Dale DC, Klebanoff SJ: Glucocorticoids inhibit apoptosis of human neutrophils. Blood 1995; 86:3181-3188
112. 112. Slotman GJ, Quinn JV, Wry PC, et al: Unopposed interleukin-1 is necessary for increased plasma cytokine and eicosanoid levels to develop in severe sepsis. Ann Surg 1997; 266:77-84
113. 113. Slotman GJ, Friedman B, Brathwaite C, et al: Interleukin-1 mediates plasma levels of eicosanoids and cytokines in patients with sepsis syndrome. Shock 1995; 4:318-323
114. 114. Koller M, Wachter P, David: A et al: Arachidonic acid induces DNA-fragmentation in human polymorphonudear neutrophil granulocytes. Inflammation 1997; 21: 463-474
115. 115. Ayala A: Lymphoid apoptosis during sepsis: Now that we've found it, what do we do with it? Crit Care Med 1997; 25:1261-1262
116. 116. Secor HV: The inflammatory/immune response in critical illness. Crit Care Nurse Clin North Am 1994; 6:309-319