Immunoparalysis after multiple trauma

Injury

Volumn 38, Issue 12, 2007, Pages 1346-1357

  Tschoeke, Sven K ^a   Ertel, Wolfgang ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Apoptosis; HO 1; Immunosuppression; T regulatory cells; Th17

Indexed keywords

INTERLEUKIN 18 RECEPTOR ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN PRESENTATION; ARTICLE; DOWN REGULATION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; MONOCYTE; MULTIPLE ORGAN FAILURE; MULTIPLE TRAUMA; NATURAL KILLER CELL; NONHUMAN; PHAGOCYTOSIS; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

CYTOKINES; HUMANS; IMMUNE SYSTEM DISEASES; IMMUNE TOLERANCE; IMMUNITY, CELLULAR; MULTIPLE TRAUMA; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; T-LYMPHOCYTES;

EID: 36549086698     PISSN: 00201383     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.injury.2007.08.041     Document Type: Article

References (118)

1. Abraham E., and Chang Y.H. Haemorrhage-induced alterations in function and cytokine production of T cells and T cell subpopulations. Clin Exp Immunol 90 (1992) 497-502
2. Akira S., and Takeda K. Toll-like receptor signalling. Nat Rev Immunol 4 (2004) 499-511
3. Akira S., Takeda K., and Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2 (2001) 675-680
4. Barshes N.R., Wyllie S., and Goss J.A. Inflammation-mediated dysfunction and apoptosis in pancreatic islet transplantation: implications for intrahepatic grafts. J Leukoc Biol 77 (2005) 587-597
5. Basta P.V., Moore T.L., Yokota S., and Ting J.P. A beta-adrenergic agonist modulates DR alpha gene transcription via enhanced cAMP levels in a glioblastoma multiforme line. J Immunol 142 (1989) 2895-2901
6. Beattie M.S. Inflammation and apoptosis: linked therapeutic targets in spinal cord injury. Trends Mol Med 10 (2004) 580-583
7. Bengmark S. Aggressive management of surgical emergencies. Ann R Coll Surg Engl 88 (2006) 624-629
8. Bettelli E., Carrier Y., Gao W., et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441 (2006) 235-238
9. Blazar B.A., Rodrick M.L., O'Mahony J.B., et al. Suppression of natural killer-cell function in humans following thermal and traumatic injury. J Clin Immunol 6 (1986) 26-36
10. Bone R.C. Immunologic dissonance: a continuing evolution in our understanding of the systemic inflammatory response syndrome (SIRS) and the multiple organ dysfunction syndrome (MODS). Ann Intern Med 125 (1996) 680-687
11. Brooks W.H., Netsky M.G., Normansell D.E., and Horwitz D.A. Depressed cell-mediated immunity in patients with primary intracranial tumors. Characterization of a humoral immunosuppressive factor. J Exp Med 136 (1972) 1631-1647
12. Buechler C., Ritter M., Orso E., et al. Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro- and antiinflammatory stimuli. J Leukoc Biol 67 (2000) 97-103
13. Cavaillon J.M., Adrie C., Fitting C., and Adib-Conquy M. Reprogramming of circulatory cells in sepsis and SIRS. J Endotoxin Res 11 (2005) 311-320
14. Celada A., and Nathan C. Macrophage activation revisited. Immunol Today 15 (1994) 100-102
15. Chauveau C., Remy S., Royer P.J., et al. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 106 (2005) 1694-1702
16. Chen C., Lee W.H., Zhong L., and Liu C.P. Regulatory T cells can mediate their function through the stimulation of APCs to produce immunosuppressive nitric oxide. J Immunol 176 (2006) 3449-3460
17. Choi B.M., Pae H.O., Jeong Y.R., et al. Critical role of heme oxygenase-1 in Foxp3-mediated immune suppression. Biochem Biophys Res Commun 327 (2005) 1066-1071
18. Cohen-Saidon C., Nechushtan H., Kahlon S., et al. A novel strategy using single-chain antibody to show the importance of Bcl-2 in mast cell survival. Blood 102 (2003) 2506-2512
19. Cua D.J., and Kastelein R.A. TGF-beta, a 'double agent' in the immune pathology war. Nat Immunol 7 (2006) 557-559
20. Danial N.N., and Korsmeyer S.J. Cell death: critical control points. Cell 116 (2004) 205-219
21. Daniel T., Alexander M., Hubbard W.J., et al. Nitric oxide contributes to the development of a post-injury Th2 T-cell phenotype and immune dysfunction. J Cell Physiol 208 (2006) 418-427
22. Delogu G., Moretti S., Antonucci A., et al. Apoptosis and surgical trauma: dysregulated expression of death and survival factors on peripheral lymphocytes. Arch Surg 135 (2000) 1141-1147
23. Docke W.D., Randow F., Syrbe U., et al. Monocyte deactivation in septic patients: restoration by IFN-gamma treatment. Nat Med 3 (1997) 678-681
24. DosReis G.A., Nobrega A.F., and de Carvalho R.P. Purinergic modulation of T-lymphocyte activation: differential susceptibility of distinct activation steps and correlation with intracellular 3′,5′-cyclic adenosine monophosphate accumulation. Cell Immunol 101 (1986) 213-231
25. Drummond G.S., and Kappas A. Prevention of neonatal hyperbilirubinemia by tin protoporphyrin IX, a potent competitive inhibitor of heme oxidation. Proc Natl Acad Sci USA 78 (1981) 6466-6470
26. Edwards III C.K., Watts L.M., Parmely M.J., et al. Effect of the carbocyclic nucleoside analogue MDL 201, 112 on inhibition of interferon-gamma-induced priming of Lewis (LEW/N) rat macrophages for enhanced respiratory burst and MHC class II Ia+ antigen expression. J Leukoc Biol 56 (1994) 133-144
27. Eipel C., Eisold M., Schuett H., and Vollmar B. Inhibition of heme oxygenase-1 protects against tissue injury in carbon tetrachloride exposed livers. J Surg Res 139 1 (2007) 113-120
28. Emmenegger U., Schaer D.J., Larroche C., and Neftel K.A. Haemophagocytic syndromes in adults: current concepts and challenges ahead. Swiss Med Wkly 135 (2005) 299-314
29. Fabriek B.O., Dijkstra C.D., and van den Berg T.K. The macrophage scavenger receptor CD163. Immunobiology 210 (2005) 153-160
30. Faist E., Kupper T.S., Baker C.C., et al. Depression of cellular immunity after major injury Its association with posttraumatic complications and its reversal with immunomodulation. Arch Surg 121 (1986) 1000-1005
31. Faunce D.E., Gamelli R.L., Choudhry M.A., and Kovacs E.J. A role for CD1d-restricted NKT cells in injury-associated T cell suppression. J Leukoc Biol 73 (2003) 747-755
32. Fukuo K., Suhara T., Nakahashi T., et al. Activated T cells induce up-regulation of Fas antigen in cultured endothelial cells. Heart Vessels Suppl. 12 (1997) 81-83
33. Furchgott R.F., Carvalho M.H., Khan M.T., and Matsunaga K. Evidence for endothelium-dependent vasodilation of resistance vessels by acetylcholine. Blood Vessels 24 (1987) 145-149
34. Furuzawa-Carballeda J., Vargas-Rojas M.I., and Cabral A.R. Autoimmune inflammation from the Th17 perspective. Autoimmun Rev 6 (2007) 169-175
35. Giannoudis P.V. Current concepts of the inflammatory response after major trauma: an update. Injury 34 (2003) 397-404
36. Gutierrez G., Reines H.D., and Wulf-Gutierrez M.E. Clinical review: hemorrhagic shock. Crit Care 8 (2004) 373-381
37. Harris S.G., Padilla J., Koumas L., et al. Prostaglandins as modulators of immunity. Trends Immunol 23 (2002) 144-150
38. Hashimoto S., Kobayashi A., Kooguchi K., et al. Upregulation of two death pathways of perforin/granzyme and FasL/Fas in septic acute respiratory distress syndrome. Am J Respir Crit Care Med 161 (2000) 237-243
39. Hasko G., Deitch E.A., Szabo C., et al. Adenosine: a potential mediator of immunosuppression in multiple organ failure. Curr Opin Pharmacol 2 (2002) 440-444
40. Hasko G., Kuhel D.G., Chen J.F., et al. Adenosine inhibits IL-12 and TNF-alpha production via adenosine A2a receptor-dependent and independent mechanisms. FASEB J 14 (2000) 2065-2074
41. Hasko G., Szabo C., Nemeth Z.H., et al. Adenosine receptor agonists differentially regulate IL-10, TNF-alpha, and nitric oxide production in RAW 264, 7 macrophages and in endotoxemic mice. J Immunol 157 (1996) 4634-4640
42. Hasko G., Szabo C., Nemeth Z.H., et al. Stimulation of beta-adrenoceptors inhibits endotoxin-induced IL-12 production in normal and IL-10 deficient mice. J Neuroimmunol 88 (1998) 57-61
43. Hotchkiss R.S., Swanson P.E., Cobb J.P., et al. Apoptosis in lymphoid and parenchymal cells during sepsis: findings in normal and T- and B-cell-deficient mice. Crit Care Med 25 (1997) 1298-1307
44. Hotchkiss R.S., Tinsley K.W., Swanson P.E., et al. Depletion of dendritic cells, but not macrophages, in patients with sepsis. J Immunol 168 (2002) 2493-2500
45. Huber S., Schramm C., Lehr H.A., et al. Cutting edge: TGF-beta signaling is required for the in vivo expansion and immunosuppressive capacity of regulatory CD4+CD25+ T cells. J Immunol 173 (2004) 6526-6531
46. Kaizu T., Tamaki T., Tanaka M., et al. Preconditioning with tin-protoporphyrin IX attenuates ischemia/reperfusion injury in the rat kidney. Kidney Int 63 (2003) 1393-1403
47. Kalinski P., Vieira P.L., Schuitemaker J.H., et al. Prostaglandin E(2) is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 97 (2001) 3466-3469
48. Ke B., Shen X.D., Zhai Y., et al. Heme oxygenase 1 mediates the immunomodulatory and antiapoptotic effects of interleukin 13 gene therapy in vivo and in vitro. Hum Gene Ther 13 (2002) 1845-1857
49. Keel M., and Trentz O. Pathophysiology of polytrauma. Injury 36 (2005) 691-709
50. Kelso A. Th1 and Th2 subsets: paradigms lost?. Immunol Today 16 (1995) 374-379
51. Kipnis J., Cardon M., Avidan H., et al. Dopamine, through the extracellular signal-regulated kinase pathway, downregulates CD4+CD25+ regulatory T-cell activity: implications for neurodegeneration. J Neurosci 24 (2004) 6133-6143
52. Koppelman B., Neefjes J.J., de Vries J.E., and de Waal Malefyt R. Interleukin-10 down-regulates MHC class II alphabeta peptide complexes at the plasma membrane of monocytes by affecting arrival and recycling. Immunity 7 (1997) 861-871
53. Kox W.J., Bone R.C., Krausch D., et al. Interferon gamma-1b in the treatment of compensatory anti-inflammatory response syndrome A new approach: proof of principle. Arch Intern Med 157 (1997) 389-393
54. Kunkel S.L., Spengler M., May M.A., et al. Prostaglandin E2 regulates macrophage-derived tumor necrosis factor gene expression. J Biol Chem 263 (1988) 5380-5384
55. Kuroki K., Takahashi H.K., Iwagaki H., et al. Beta2-adrenergic receptor stimulation-induced immunosuppressive effects possibly through down-regulation of co-stimulatory molecules, ICAM-1, CD40 and CD14 on monocytes. J Int Med Res 32 (2004) 465-483
56. Le Moine O., Stordeur P., Schandene L., et al. Adenosine enhances IL-10 secretion by human monocytes. J Immunol 156 (1996) 4408-4414
57. Li Q., Li J., Zhang L., et al. Preconditioning with hyperbaric oxygen induces tolerance against oxidative injury via increased expression of heme oxygenase-1 in primary cultured spinal cord neurons. Life Sci 80 (2007) 1087-1093
58. MacConmara M.P., Maung A.A., Fujimi S., et al. Increased CD4+ CD25+ T regulatory cell activity in trauma patients depresses protective Th1 immunity. Ann Surg 244 (2006) 514-523
59. Madden K.S., Sanders V.M., and Felten D.L. Catecholamine influences and sympathetic neural modulation of immune responsiveness. Annu Rev Pharmacol Toxicol 35 (1995) 417-448
60. Mandron M., Aries M.F., Brehm R.D., et al. Human dendritic cells conditioned with Staphylococcus aureus enterotoxin B promote TH2 cell polarization. J Allergy Clin Immunol 117 (2006) 1141-1147
61. Mangan P.R., Harrington L.E., O'Quinn D.B., et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441 (2006) 231-234
62. McCall T.B., Boughton-Smith N.K., Palmer R.M., et al. Synthesis of nitric oxide from L-arginine by neutrophils Release and interaction with superoxide anion. Biochem J 261 (1989) 293-296
63. Menger M.D., and Vollmar B. Surgical trauma: hyperinflammation versus immunosuppression?. Langenbecks Arch Surg 389 (2004) 475-484
64. Menges T., Engel J., Welters I., et al. Changes in blood lymphocyte populations after multiple trauma: association with posttraumatic complications. Crit Care Med 27 (1999) 733-740
65. Miura N., Yamamoto M., Fukutake M., et al. Anti-CD3 induces bi-phasic apoptosis in murine intestinal epithelial cells: possible involvement of the Fas/Fas ligand system in different T cell compartments. Int Immunol 17 (2005) 513-522
66. Mohri T., Ogura H., Koh T., et al. Enhanced expression of intracellular heme oxygenase-1 in deactivated monocytes from patients with severe systemic inflammatory response syndrome. J Trauma 61 (2006) 616-623
67. Molina P.E. Noradrenergic inhibition of TNF upregulation in hemorrhagic shock. Neuroimmunomodulation 9 (2001) 125-133
68. Moller H.J., Moestrup S.K., Weis N., et al. Macrophage serum markers in pneumococcal bacteremia: prediction of survival by soluble CD163. Crit Care Med 34 (2006) 2561-2566
69. Monneret G., Debard A.L., Venet F., et al. Marked elevation of human circulating CD4+CD25+ regulatory T cells in sepsis-induced immunoparalysis. Crit Care Med 31 (2003) 2068-2071
70. Moodycliffe A.M., Nghiem D., Clydesdale G., and Ullrich S.E. Immune suppression and skin cancer development: regulation by NKT cells. Nat Immunol 1 (2000) 521-525
71. Mosmann T.R., and Sad S. The expanding universe of T-cell subsets: Th1 and Th2 and more. Immunol Today 17 (1996) 138-146
72. Nakae S., Iwakura Y., Suto H., and Galli S.J. Phenotypic differences between Th1 and Th17 cells and negative regulation of Th1 cell differentiation by IL-17. J Leukoc Biol 81 5 (2007) 1258-1268
73. Nakamichi I., Habtezion A., Zhong B., et al. Hemin-activated macrophages home to the pancreas and protect from acute pancreatitis via heme oxygenase-1 induction. J Clin Invest 115 (2005) 3007-3014
74. Nakamura K., Kitani A., Fuss I., et al. TGF-beta 1 plays an important role in the mechanism of CD4+CD25+ regulatory T cell activity in both humans and mice. J Immunol 172 (2004) 834-842
75. Nakos G., Malamou-Mitsi V.D., Lachana A., et al. Immunoparalysis in patients with severe trauma and the effect of inhaled interferon-gamma. Crit Care Med 30 (2002) 1488-1494
76. Neff T.A., Guo R.F., Neff S.B., et al. Relationship of acute lung inflammatory injury to Fas/FasL system. Am J Pathol 166 (2005) 685-694
77. Ni Choileain N., MacConmara M., Zang Y., et al. Enhanced regulatory T cell activity is an element of the host response to injury. J Immunol 176 (2006) 225-236
78. Oberholzer A., Oberholzer C., Minter R.M., and Moldawer L.L. Considering immunomodulatory therapies in the septic patient: should apoptosis be a potential therapeutic target?. Immunol Lett 75 (2001) 221-224
79. Oberholzer C., Oberholzer A., Clare-Salzler M., and Moldawer L.L. Apoptosis in sepsis: a new target for therapeutic exploration. FASEB J 15 (2001) 879-892
80. Palmer J.L., Tulley J.M., Kovacs E.J., et al. Injury-induced suppression of effector T cell immunity requires CD1d-positive APCs and CD1d-restricted NKT cells. J Immunol 177 (2006) 92-99
81. Panina-Bordignon P., Mazzeo D., Lucia P.D., et al. Beta2-agonists prevent Th1 development by selective inhibition of interleukin 12. J Clin Invest 100 (1997) 1513-1519
82. Papathanassoglou E.D., Moynihan J.A., McDermott M.P., and Ackerman M.H. 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 (2001) 709-718
83. Pavlov V.A., Wang H., Czura C.J., et al. The cholinergic anti-inflammatory pathway: a missing link in neuroimmunomodulation. Mol Med 9 (2003) 125-134
84. Pioli P.A., Goonan K.E., Wardwell K., and Guyre P.M. TGF-beta regulation of human macrophage scavenger receptor CD163 is Smad3-dependent. J Leukoc Biol 76 (2004) 500-508
85. Rabehi L., Irinopoulou T., Cholley B., et al. Gram-positive and gram-negative bacteria do not trigger monocytic cytokine production through similar intracellular pathways. Infect Immun 69 (2001) 4590-4599
86. Raghupathi R. Cell death mechanisms following traumatic brain injury. Brain Pathol 14 (2004) 215-222
87. Riedemann N.C., Guo R.F., and Ward P.A. The enigma of sepsis. J Clin Invest 112 (2003) 460-467
88. Roszman T., Elliott L., and Brooks W. Modulation of T-cell function by gliomas. Immunol Today 12 (1991) 370-374
89. Schaer D.J., Schaer C.A., Schoedon G., et al. Hemophagocytic macrophages constitute a major compartment of heme oxygenase expression in sepsis. Eur J Haematol 77 (2006) 432-436
90. Scheel-Toellner D., Wang K., Craddock R., et al. Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood 104 (2004) 2557-2564
91. Schwiebert L.M., Schleimer R.P., Radka S.F., and Ono S.J. Modulation of MHC class II expression in human cells by dexamethasone. Cell Immunol 165 (1995) 12-19
92. Shimizu T., Kawamura T., Miyaji C., et al. Resistance of extrathymic T cells to stress and the role of endogenous glucocorticoids in stress associated immunosuppression. Scand J Immunol 51 (2000) 285-292
93. Shinomiya S., Naraba H., Ueno A., et al. Regulation of TNFalpha and interleukin-10 production by prostaglandins I(2) and E(2): studies with prostaglandin receptor-deficient mice and prostaglandin E-receptor subtype-selective synthetic agonists. Biochem Pharmacol 61 (2001) 1153-1160
94. Shokawa T., Yoshizumi M., Yamamoto H., et al. Induction of heme oxygenase-1 inhibits monocyte chemoattractant protein-1 mRNA expression in U937 cells. J Pharmacol Sci 100 (2006) 162-166
95. Siner J.M., Jiang G., Cohen Z.I., et al. VEGF-induced heme oxygenase-1 confers cytoprotection from lethal hyperoxia in vivo. FASEB J 21 7 (2007) 1422-1432
96. Spierings D., McStay G., Saleh M., et al. Connected to death: the (unexpurgated) mitochondrial pathway of apoptosis. Science 310 (2005) 66-67
97. Spolarics Z., Siddiqi M., Siegel J.H., et al. Depressed interleukin-12-producing activity by monocytes correlates with adverse clinical course and a shift toward Th2-type lymphocyte pattern in severely injured male trauma patients. Crit Care Med 31 (2003) 1722-1729
98. Strassmann G., Patil-Koota V., Finkelman F., et al. Evidence for the involvement of interleukin 10 in the differential deactivation of murine peritoneal macrophages by prostaglandin E2. J Exp Med 180 (1994) 2365-2370
99. Szondy Z. Adenosine stimulates DNA fragmentation in human thymocytes by Ca(2+)-mediated mechanisms. Biochem J 304 (1994) 877-885
100. Thivierge M., Stankova J., and Rola-Pleszczynski M. Toll-like receptor agonists differentially regulate cysteinyl-leukotriene receptor 1 expression and function in human dendritic cells. J Allergy Clin Immunol 117 (2006) 1155-1162
101. Tracey K.J. The inflammatory reflex. Nature 420 (2002) 853-859
102. Varga C., Laszlo F., Fritz P., et al. Modulation by heme and zinc protoporphyrin of colonic heme oxygenase-1 and experimental inflammatory bowel disease in the rat. Eur J Pharmacol 561 1-3 (2007) 164-171
103. Venet F., Pachot A., Debard A.L., et al. Increased percentage of CD4+CD25+ regulatory T cells during septic shock is due to the decrease of CD4+CD25- lymphocytes. Crit Care Med 32 (2004) 2329-2331
104. Venet F., Pachot A., Debard A.L., et al. Human CD4+CD25+ regulatory T lymphocytes inhibit lipopolysaccharide-induced monocyte survival through a Fas/Fas ligand-dependent mechanism. J Immunol 177 (2006) 6540-6547
105. Walker W., and Rotondo D. Prostaglandin E2 is a potent regulator of interleukin-12- and interleukin-18-induced natural killer cell interferon-gamma synthesis. Immunology 111 (2004) 298-305
106. Watanabe Y., Lee S., and Allison A.C. Control of the expression of a class II major histocompatibility gene (HLA-DR) in various human cell types: down-regulation by IL-1 but not by IL-6, prostaglandin E2, or glucocorticoids. Scand J Immunol 32 (1990) 601-609
107. Weaver C.T., Harrington L.E., Mangan P.R., et al. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 24 (2006) 677-688
108. Weaver L.K., Hintz-Goldstein K.A., Pioli P.A., et al. Pivotal advance: activation of cell surface Toll-like receptors causes shedding of the hemoglobin scavenger receptor CD163. J Leukoc Biol 80 (2006) 26-35
109. Weaver L.K., Pioli P.A., Wardwell K., et al. Up-regulation of human monocyte CD163 upon activation of cell-surface Toll-like receptors. J Leukoc Biol 81 (2007) 663-671
110. Wesche D.E., Lomas-Neira J.L., Perl M., et al. Leukocyte apoptosis and its significance in sepsis and shock. J Leukoc Biol 78 (2005) 325-337
111. Weyrich A.S., Ma X.L., and Lefer A.M. The role of L-arginine in ameliorating reperfusion injury after myocardial ischemia in the cat. Circulation 86 (1992) 279-288
112. Woiciechowsky C., Asadullah K., Nestler D., et al. Sympathetic activation triggers systemic interleukin-10 release in immunodepression induced by brain injury. Nat Med 4 (1998) 808-813
113. Wolk K., Docke W., von Baehr V., et al. Comparison of monocyte functions after LPS- or IL-10-induced reorientation: importance in clinical immunoparalysis. Pathobiology 67 (1999) 253-256
114. Wysocka M., Montaner L.J., and Karp C.L. Flt3 ligand treatment reverses endotoxin tolerance-related immunoparalysis. J Immunol 174 (2005) 7398-7402
115. Xia Z.W., Zhong W.W., Xu L.Q., et al. Heme oxygenase-1-mediated CD4+CD25high regulatory T cells suppress allergic airway inflammation. J Immunol 177 (2006) 5936-5945
116. Zhang L., Yi H., Xia X.P., and Zhao Y. Transforming growth factor-beta: an important role in CD4+CD25+ regulatory T cells and immune tolerance. Autoimmunity 39 (2006) 269-276
117. Zhang X., Chen Y., Jenkins L.W., et al. Bench-to-bedside review: apoptosis/programmed cell death triggered by traumatic brain injury. Crit Care 9 (2005) 66-75
118. Zimmermann K.C., and Green D.R. How cells die: apoptosis pathways. J Allergy Clin Immunol 108 (2001) S99-S103