T cells are potent early mediators of the host response to sepsis

Shock

Volumn 34, Issue 4, 2010, Pages 327-336

  Kasten, Kevin R ^a   Tschöp, Johannes ^a,b   Adediran, Samuel G ^a   Hildeman, David A ^c   Caldwell, Charles C ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

apoptosis; IL 17; interferon ; Sepsis; T cells

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17;

ADAPTIVE IMMUNITY; APOPTOSIS; CELL SURVIVAL; DISEASE SEVERITY; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; LYMPHOCYTE; MORBIDITY; MORTALITY; NONHUMAN; REVIEW; SEPSIS; T LYMPHOCYTE;

ANIMALS; APOPTOSIS; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-17; SEPSIS; T-LYMPHOCYTES;

EID: 77957698207     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/SHK.0b013e3181e14c2e     Document Type: Review

References (135)

1. Brooks HF, Osabutey CK, Moss RF, Andrews PL, Davies DC: Caecal ligation and puncture in the rat mimics the pathophysiological changes in human sepsis and causes multi-organ dysfunction. Metab Brain Dis 22:353-373, 2007.
2. Crouser E, Exline M, Knoell D, Wewers MD: Sepsis: links between pathogen sensing and organ damage. Curr Pharm Des 14:1840-1852, 2008.
3. Hietbrink F, Koenderman L, Rijkers G, Leenen L: Trauma: the role of the innate immune system. World J Emerg Surg 1:15, 2006.
4. Cohen J: The immunopathogenesis of sepsis. Nature 420:885-891, 2002.
5. Faist E, Kim C: Therapeutic immunomodulatory approaches for the control of systemic inflammatory response syndrome and the prevention of sepsis. New Horiz 6:97-102, 1998.
6. Baue AE, Durham R, Faist E: Systemic inflammatory response syndrome (SIRS), multiple organ dysfunction syndrome (MODS), multiple organ failure (MOF): are we winning the battle? Shock 10:79-89, 1998.
7. Rittirsch D, Hoesel LM, Ward PA: The disconnect between animal models of sepsis and human sepsis. J Leukoc Biol 81:137-143, 2007.
8. + T lymphocytes in humans. J Immunol 166:6952-6963, 2001.
9. Wesche DE, Lomas-Neira JL, Perl M, Chung CS, Ayala A: Leukocyte apoptosis and its significance in sepsis and shock. J Leukoc Biol 78:325-337, 2005.
10. Bandyopadhyay G, De A, Laudanski K, Li F, Lentz C, Bankey P, Miller-Graziano C: Negative signaling contributes to T-cell anergy in trauma patients. Crit Care Med 35:794-801, 2007.
11. Cheadle WG, Pemberton RM, Robinson D, Livingston DH, Rodriguez JL, Polk HC Jr: Lymphocyte subset responses to trauma and sepsis. J Trauma 35:844-849, 1993.
12. Chang KC, Unsinger J, Davis CG, Schwulst SJ, Muenzer JT, Strasser A, Hotchkiss RS: Multiple triggers of cell death in sepsis: death receptor and mitochondrial-mediated apoptosis. FASEB J 21:708-719, 2007.
13. Hotchkiss RS, Swanson PE, Freeman BD, Tinsley KW, Cobb JP, Matuschak GM, Buchman TG, Karl IE: Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit Care Med 27:1230-1251, 1999.
14. Spolarics Z, Siddiqi M, Siegel JH, Garcia ZC, Stein DS, Denny T, Deitch EA: Depressed interleukin-12Yproducing 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 31:1722-1729, 2003.
15. Rajan G, Sleigh JW: Lymphocyte counts and the development of nosocomial sepsis. Intensive Care Med 23:1187, 1997.
16. Hotchkiss RS, Swanson PE, Knudson CM, Chang KC, Cobb JP, Osborne DF, Zollner KM, Buchman TG, Korsmeyer SJ, Karl IE: Overexpression of Bcl-2 in transgenic mice decreases apoptosis and improves survival in sepsis. J Immunol 162:4148-4156, 1999.
17. Miller AC, Rashid RM, Elamin EM: The BT[in trauma: the helper T-cell response and the role of immunomodulation in trauma and burn patients. J Trauma 63:1407-1417, 2007.
18. Sallusto F, Geginat J, Lanzavecchia A: Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 22:745-763, 2004.
19. + T cells have a distinct transcriptional response six hours after the onset of sepsis. J Am Coll Surg 203:365-375, 2006.
20. Hsieh CS, Zheng Y, Liang Y, Fontenot JD, Rudensky AY: An intersection between the self-reactive regulatory and nonregulatory T cell receptor repertoires. Nat Immunol 7:401-410, 2006.
21. Lages CS, Suffia I, Velilla PA, Huang B, Warshaw G, Hildeman DA, Belkaid Y, Chougnet C: Functional regulatory T cells accumulate in aged hosts and promote chronic infectious disease reactivation. J Immunol 181:1835-1848, 2008.
22. Ai YH, Yao YM, Dai XG: Effect of apoptosis of CD4+ CD25+ regulatory T cells on proliferation as well as secretion of effector T cells and interven-tional activity of Xuebijing injection in septic rats [In Chinese]. Zhonghua Wai Ke Za Zhi 47:58-61, 2009.
23. Venet F, Chung CS, Kherouf H, Geeraert A, Malcus C, Poitevin F, Bohe J, Lepape A, Ayala A, Monneret G: Increased circulating regulatory T cells (CD4(+)CD25(+)CD127(j)) contribute to lymphocyte anergy in septic shock patients. Intensive Care Med 35:678-686, 2009.
24. Wisnoski N, Chung CS, Chen Y, Huang X, Ayala A: The contribution of CD4+ CD25+ T-regulatory-cells to immune suppression in sepsis. Shock 27:251-257, 2007.
25. Hakem R, Hakem A, Duncan GS, Henderson JT, Woo M, Soengas MS, Elia A, De la Pompa JL, Kagi D, Khoo W, et al.: Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 94:339-352, 1998.
26. Ma T, Han L, Gao Y, Li L, Shang X, Hu W, Xue C: The endoplasmic retic-ulum stressYmediated apoptosis signal pathway is involved in sepsis-induced abnormal lymphocyte apoptosis. Eur Surg Res 41:219-225, 2008.
27. Pinheiro da Silva F, Nizet V: Cell death during sepsis: integration of disintegration in the inflammatory response to overwhelming infection. Apop-tosis 14:509-521, 2009.
28. Hotchkiss RS, Strasser A, McDunn JE, Swanson PE: Cell death. N Engl J Med 361:1570-1583, 2009.
29. Ashkenazi A: Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat Rev Cancer 2:420-430, 2002.
30. Graham RM, Thompson JW, Wei J, Bishopric NH, Webster KA: Regulation of Bnip3 death pathways by calcium, phosphorylation, and hypoxia-reoxygenation. Antioxid Redox Signal 9:1309-1315, 2007.
31. Yu J, Zhang L: The transcriptional targets of p53 in apoptosis control. Bio-chem Biophys Res Commun 331:851-858, 2005.
32. Kang MH, Reynolds CP: Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy. Clin Cancer Res 15:1126-1132, 2009.
33. Bouillet P, O'Reilly LA: CD95, BIM and T cell homeostasis. Nat Rev Immunol 9:514-519, 2009.
34. Schwulst SJ, Muenzer JT, Peck-Palmer OM, Chang KC, Davis CG, McDonough JS, Osborne DF, Walton AH, Unsinger J, McDunn JE, et al.: Bim siRNA decreases lymphocyte apoptosis and improves survival in sepsis. Shock 30:127-134, 2008.
35. Hildeman DA, Zhu Y, Mitchell TC, Bouillet P, Strasser A, Kappler J, Marrack P: Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity 16:759-767, 2002.
36. Weber SU, Schewe JC, Lehmann LE, Muller S, Book M, Klaschik S, Hoeft A, Stuber F: Induction of Bim and Bid gene expression during accelerated apoptosis in severe sepsis. Crit Care 12:R128, 2008.
37. Hotchkiss RS, McConnell KW, Bullok K, Davis CG, Chang KC, Schwulst SJ, Dunne JC, Dietz GP, Bahr M, McDunn JE, et al.: TAT-BH4 and TAT-Bcl-xL peptides protect against sepsis-induced lymphocyte apoptosis in vivo. J Immunol 176:5471-5477, 2006.
38. Zhai D, Jin C, Huang Z, Satterthwait AC, Reed JC: Differential regulation of Bax and Bak by anti-apoptotic Bcl-2 family proteins Bcl-B and Mcl-1. J Biol Chem 283:9580-9586, 2008.
39. Tinsley KW, Cheng SL, Buchman TG, Chang KC, Hui JJ, Swanson PE, Karl IE, Hotchkiss RS: Caspases-2,-3,-6, and-9, but not caspase-1, are activated in sepsis-induced thymocyte apoptosis. Shock 13:1-7, 2000.
40. Ghobrial IM, Witzig TE, Adjei AA: Targeting apoptosis pathways in cancer therapy. CA Cancer J Clin 55:178-194, 2005.
41. Fulda S, Debatin KM: Extrinsic versus intrinsic apoptosis pathways in anti-cancer chemotherapy. Oncogene 25:4798-4811, 2006.
42. Debatin KM, Krammer PH: Death receptors in chemotherapy and cancer. Oncogene 23:2950-2966, 2004.
43. Schimmer AD: Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res 64:7183-7190, 2004.
44. Zhang J, Zhang D, Hua Z: FADD and its phosphorylation. IUBMB Life 56:395-401, 2004.
45. Su H, Bidere N, Zheng L, Cubre A, Sakai K, Dale J, Salmena L, Hakem R, Straus S, Lenardo M: Requirement for caspase-8 in NF-kappaB activation by antigen receptor. Science 307:1465-1468, 2005.
46. Wesche-Soldato DE, Chung CS, Lomas-Neira J, Doughty LA, Gregory SH, Ayala A: In vivo delivery of caspase-8 or Fas siRNA improves the survival of septic mice. Blood 106:2295-2301, 2005.
47. Kaufman RJ: Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13:1211-1233, 1999.
48. Ferri KF, Kroemer G: Organelle-specific initiation of cell death pathways. Nat Cell Biol 3:E255YE263, 2001.
49. Jimbo A, Fujita E, Kouroku Y, Ohnishi J, Inohara N, Kuida K, Sakamaki K, Yonehara S, Momoi T: ER stress induces caspase-8 activation, stimulating cytochrome c release and caspase-9 activation. Exp Cell Res 283:156-166, 2003.
50. Saleh M, Mathison JC, Wolinski MK, Bensinger SJ, Fitzgerald P, Droin N, Ulevitch RJ, Green DR, Nicholson DW: Enhanced bacterial clearance and sepsis resistance in caspase-12Ydeficient mice. Nature 440:1064-1068, 2006.
51. Oakes SA, Lin SS, Bassik MC: The control of endoplasmic reticulum-initiated apoptosis by the BCL-2 family of proteins. Curr Mol Med 6:99-109, 2006.
52. Hetz CA: ER stress signaling and the BCL-2 family of proteins: from adaptation to irreversible cellular damage. Antioxid Redox Signal 9:2345-2355, 2007.
53. Roy S, Nicholson DW: Cross-talk in cell death signaling. J Exp Med 192:21-26, 2000.
54. Veresov VG, Davidovskii AI: Monte Carlo simulations of tBid association with the mitochondrial outer membrane. Eur Biophys J 37:19-33, 2007.
55. Hotchkiss RS, Nicholson DW: Apoptosis and caspases regulate death and inflammation in sepsis. Nat Rev Immunol 6:813-822, 2006.
56. Hotchkiss RS, Chang KC, Grayson MH, Tinsley KW, Dunne BS, Davis CG, Osborne DF, Karl IE: 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, 2003.
57. Vandenabeele P, Vanden Berghe T, Festjens N: Caspase inhibitors promote alternative cell death pathways. Sci STKE 2006:pe44, 2006.
58. Hotchkiss RS, Tinsley KW, Swanson PE, Chang KC, Cobb JP, Buchman TG, Korsmeyer SJ, Karl IE: Prevention of lymphocyte cell death in sepsis improves survival in mice. Proc Natl Acad Sci\USA 96:14541-14546, 1999.
59. Qin S, Wang H, Yuan R, Li H, Ochani M, Ochani K, Rosas-Ballina M, Czura CJ, Huston JM, Miller E, et al.: Role of HMGB1 in apoptosis-mediated sepsis lethality. J Exp Med 203:1637-1642, 2006.
60. Brahmamdam P, Watanabe E, Unsinger J, Chang KC, Schierding W, Hoekzema AS, Zhou TT, McDonough JS, Holemon H, Heidel JD, et al.: Targeted delivery of siRNA to cell death proteins in sepsis. Shock 32:131-139, 2009.
61. Chung CS, Xu YX, Wang W, Chaudry IH, Ayala A: Is Fas ligand or endotoxin responsible for mucosal lymphocyte apoptosis in sepsis? Arch Surg 133: 1213-1220, 1998.
62. Hiramatsu M, Hotchkiss RS, Karl IE, Buchman TG: Cecal ligation and puncture (CLP) induces apoptosis in thymus, spleen, lung, and gut by an endotoxin and TNF-independent pathway. Shock 7:247-253, 1997.
63. Sun H, Gong S, Carmody RJ, Hilliard A, Li L, Sun J, Kong L, Xu L, Hilliard B, Hu S, et al.: TIPE2, a negative regulator of innate and adaptive immunity that maintains immune homeostasis. Cell 133:415-426, 2008.
64. Ayala A, Deol ZK, Lehman DL, Herdon CD, Chaudry IH: Polymicrobial sepsis but not low-dose endotoxin infusion causes decreased splenocyte IL-2/IFN-gamma release while increasing IL-4/IL-10 production. J Surg Res 56: 579-585, 1994.
65. Gough DB, Jordan A, Mannick JA, Rodrick MI: Impaired cell-mediated immunity in experimental abdominal sepsis and the effect of interleukin 2. Arch Surg 127:859-863, 1992.
66. + T cell responses. J Immunol 178:4027-4031, 2007.
67. Dias S, Silva H Jr, Cumano A, Vieira P: Interleukin-7 is necessary to maintain the B cell potential in common lymphoid progenitors. J Exp Med 201: 971-979, 2005.
68. Unsinger J, McGlynn M, Kasten KR, Hoekzema AS, Watanabe E, Muenzer JT, McDonough JS, Tschop J, Ferguson TA, McDunn JE, et al.: IL-7 promotes T cell viability, trafficking, functionality and improves survival in sepsis. J Immunol 184:3768-3779, 2010.
69. Sereti I, Dunham RM, Spritzler J, Aga E, Proschan MA, Medvik K, Battaglia CA, Landay AL, Pahwa S, Fischl MA, et al.: IL-7 administration drives T cell-cycle entry and expansion in HIV-1 infection. Blood 113:6304-6314, 2009.
70. Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL, Ramsay G: 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med 31:1250-1256, 2003. (Pubitemid 36444440)
71. + T-regulatory cells. J Immunother 29:313-319, 2006.
72. Sportes C, Hakim FT, Memon SA, Zhang H, Chua KS, Brown MR, Fleisher TA, Krumlauf MC, Babb RR, Chow CK, et al.: Administration of rhIL-7 in humans increases in vivo TCR repertoire diversity by preferential expansion of naive T cell subsets. J Exp Med 205:1701-1714, 2008.
73. Hiromatsu T, Yajima T, Matsuguchi T, Nishimura H, Wajjwalku W, Arai T, Nimura Y, Yoshikai Y: Overexpression of interleukin-15 protects against Escherichia coliYinduced shock accompanied by inhibition of tumor necrosis factor-alphaYinduced apoptosis. J Infect Dis 187:1442-1451, 2003.
74. Naora H, Gougeon ML: Interleukin-15 is a potent survival factor in the prevention of spontaneous but not CD95-induced apoptosis in CD4 and CD8 T lymphocytes of HIV-infected individuals. Correlation with its ability to increase BCL-2 expression. Cell Death Differ 6:1002-1011, 1999.
75. Inoue S, Unsinger J, Davis CG, Muenzer JT, Ferguson TA, Chang K, Osborne DF, Clark AT, Coopersmith CM, McDunn JE, et al.: IL-15 prevents apoptosis, reverses innate and adaptive immune dysfunction, and improves survival in sepsis. J Immunol 184:1401-1409, 2009.
76. Orinska Z, Maurer M, Mirghomizadeh F, Bulanova E, Metz M, Nashkevich N, Schiemann F, Schulmistrat J, Budagian V, Giron-Michel J, et al.: IL-15 constrains mast cellYdependent antibacterial defenses by suppressing chymase activities. Nat Med 13:927-934, 2007.
77. Ward PA: The curiosity of IL-15. Nat Med 13:903-904, 2007.
78. Reche PA, Soumelis V, Gorman DM, Clifford T, Liu M, Travis M, Zurawski SM, Johnston J, Liu YJ, Spits H, et al.: Human thymic stromal lymphopoietin preferentially stimulates myeloid cells. J Immunol 167:336-343, 2001.
79. Soumelis V, Reche PA, Kanzler H, Yuan W, Edward G, Homey B, Gilliet M, Ho S, Antonenko S, Lauerma A, et al.: Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol 3:673-680, 2002.
80. Ying S, O'Connor B, Ratoff J, Meng Q, Mallett K, Cousins D, Robinson D, Zhang G, Zhao J, Lee TH, et al.: Thymic stromal lymphopoietin expression is increased in asthmatic airways and correlates with expression of Th2-attracting chemokines and disease severity. J Immunol 174:8183-8190, 2005.
81. Lenardo M, Chan KM, Hornung F, McFarland H, Siegel R, Wang J, Zheng L: Mature T lymphocyte apoptosisVimmune regulation in a dynamic and unpredictable antigenic environment. Annu Rev Immunol 17:221-253, 1999.
82. Swan R, Chung CS, Albina J, Cioffi W, Perl M, Ayala A: Polymicrobial sepsis enhances clearance of apoptotic immune cells by splenic macrophages. Surgery 142:253-261, 2007.
83. Savill J, Fadok V, Henson P, Haslett C: Phagocyte recognition of cells undergoing apoptosis. Immunol Today 14:131-136, 1993.
84. Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RA, Henson PM: A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405:85-90, 2000.
85. Hoffmann PR, deCathelineau AM, Ogden CA, Leverrier Y, Bratton DL, Daleke DL, Ridley AJ, Fadok VA, Henson PM: Phosphatidylserine (PS) induces PS receptorYmediated macropinocytosis and promotes clearance of apoptotic cells. J Cell Biol 155:649-659, 2001.
86. Savill J, Dransfield I, Hogg N, Haslett C: Vitronectin receptorYmediated phagocytosis of cells undergoing apoptosis. Nature 343:170-173, 1990.
87. Savill J, Hogg N, Ren Y, Haslett C: Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J Clin Invest 90:1513-1522, 1992.
88. Stern M, Savill J, Haslett C: Human monocyte-derived macrophage phagocytosis of senescent eosinophils undergoing apoptosis. Mediation by alpha v beta 3/CD36/thrombospondin recognition mechanism and lack of phlogistic response. Am J Pathol 149:911-921, 1996.
89. Devitt A, Moffatt OD, Raykundalia C, Capra JD, Simmons DL, Gregory CD: Human CD14 mediates recognition and phagocytosis of apoptotic cells. Nature 392:505-509, 1998.
90. Platt N, Suzuki H, Kurihara Y, Kodama T, Gordon S: Role for the class A macrophage scavenger receptor in the phagocytosis of apoptotic thymocytes in vitro. Proc Natl Acad Sci\USA 93:12456-12460, 1996.
91. Fukasawa M, Adachi H, Hirota K, Tsujimoto M, Arai H, Inoue K: SRB1, a class B scavenger receptor, recognizes both negatively charged liposomes and apoptotic cells. Exp Cell Res 222:246-250, 1996.
92. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM: Macrophages that have ingested apoptotic cells in vitro inhibit proinflam-matory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 101:890-898, 1998.
93. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I: Immu-nosuppressive effects of apoptotic cells. Nature 390:350-351, 1997.
94. Bzowska M, Guzik K, Barczyk K, Ernst M, Flad HD, Pryjma J: Increased IL-10 production during spontaneous apoptosis of monocytes. Eur J Immunol 32:2011-2020, 2002.
95. Gerber JS, Mosser DM: Reversing lipopolysaccharide toxicity by ligating the macrophage Fc gamma receptors. J Immunol 166:6861-6868, 2001.
96. Mosser DM: The many faces of macrophage activation. J Leukoc Biol 73:209-212, 2003.
97. Martignoni A, Tschop J, Goetzman HS, Choi LG, Reid MD, Johannigman JA, Lentsch AB, Caldwell CC: CD4-expressing cells are early mediators of the innate immune system during sepsis. Shock 29:591-597, 2008.
98. Enoh VT, Lin SH, Etogo A, Lin CY, Sherwood ER: CD4+ T-cell depletion is not associated with alterations in survival, bacterial clearance, and inflammation after cecal ligation and puncture. Shock 29:56-64, 2008.
99. + T lymphocytes. J Immunol 177:4962-4965, 2006.
100. Thiel M, Caldwell CC, Kreth S, Kuboki S, Chen P, Smith P, Ohta A, Lentsch AB, Lukashev D, Sitkovsky MV: Targeted deletion of HIF-1alpha gene in T cells prevents their inhibition in hypoxic inflamed tissues and improves septic mice survival. PLoS One 2:e853, 2007.
101. Aggarwal S, Ghilardi N, Xie MH, De Sauvage FJ, Gurney AL: Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 278:1910-1914, 2003.
102. Stockinger B, Veldhoen M, Martin B: Th17 T cells: linking innate and adaptive immunity. Semin Immunol 19:353-361, 2007.
103. Boniface K, Blom B, Liu YJ, De Waal Malefyt R: From interleukin-23 to T-helper 17 cells: human T-helper cell differentiation revisited. Immunol Rev 226:132-146, 2008.
104. Korn T, Bettelli E, Oukka M, Kuchroo VK: IL-17 and Th17 cells. Annu Rev Immunol 27:485-517, 2009.
105. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK: Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441:235-238, 2006.
106. Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, Elson CO, Hatton RD, Wahl SM, Schoeb TR, Weaver CT: Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441:231-234, 2006.
107. Verreck FA, De Boer T, Langenberg DM, Hoeve MA, Kramer M, Vaisberg E, Kastelein R, Kolk A, De Waal-Malefyt R, Ottenhoff TH: Human IL-23Yproducing type 1 macrophages promote but IL-10Yproducing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci\USA 101:4560-4565, 2004.
108. Fuss IJ, Becker C, Yang Z, Groden C, Hornung RL, Heller F, Neurath MF, Strober W, Mannon PJ: Both IL-12p70 and IL-23 are synthesized during active Crohn's disease and are down-regulated by treatment with antiYIL-12 p40 monoclonal antibody. Inflamm Bowel Dis 12:9-15, 2006.
109. Langrish CL, McKenzie BS, Wilson NJ, De Waal Malefyt R, Kastelein RA, Cua DJ: IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol Rev 202:96-105, 2004.
110. Roark CL, Simonian PL, Fontenot AP, Born WK, O'Brien RL: Gammadelta T cells: an important source of IL-17. Curr Opin Immunol 20:353-357, 2008.
111. Lee YK, Turner H, Maynard CL, Oliver JR, Chen D, Elson CO, Weaver CT: Late developmental plasticity in the T helper 17 lineage. Immunity 30:92-107, 2009.
112. Lexberg MH, Taubner A, Forster A, Albrecht I, Richter A, Kamradt T, Radbruch A, Chang HD: Th memory for interleukin-17 expression is stable in vivo. Eur J Immunol 38:2654-2664, 2008.
113. Zhou L, Ivanov II, Spolski R, Min R, Shenderov K, Egawa T, Levy DE, Leonard WJ, Littman DR: IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 8:967-974, 2007.
114. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, Cua DJ, Littman DR: The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133, 2006.
115. Yang XO, Panopoulos AD, Nurieva R, Chang SH, Wang D, Watowich SS, Dong C: STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem 282:9358-9363, 2007.
116. Lee YK, Mukasa R, Hatton RD, Weaver CT: Developmental plasticity of Th17 and Treg cells. Curr Opin Immunol 21:274-280, 2009.
117. Zhu J, Paul WE: Heterogeneity and plasticity of T helper cells. Cell Res 20:4-12, 2010.
118. Kastelein RA, Hunter CA, Cua DJ: Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation. Annu Rev Immunol 25:221-242, 2007.
119. Freitas A, Alves-Filho JC, Victoni T, Secher T, Lemos HP, Sonego F, Cunha FQ, Ryffel B: IL-17 receptor signaling is required to control polymicrobial sepsis. J Immunol 182:7846-7854, 2009.
120. Flierl MA, Rittirsch D, Gao H, Hoesel LM, Nadeau BA, Day DE, Zetoune FS, Sarma JV, Huber-Lang MS, Ferrara JL, et al.: Adverse functions of IL-17A in experimental sepsis. FASEB J 22:2198-2205, 2008.
121. Umemura M, Kawabe T, Shudo K, Kidoya H, Fukui M, Asano M, Iwakura Y, Matsuzaki G, Imamura R, Suda T: Involvement of IL-17 in Fas ligand-induced inflammation. Int Immunol 16:1099-1108, 2004.
122. Shibata K, Yamada H, Hara H, Kishihara K, Yoshikai Y: Resident Vdelta1+ gammadelta T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J Immunol 178:4466-4472, 2007.
123. Xu R, Wang R, Han G, Wang J, Chen G, Wang L, Li X, Guo R, Shen B, Li Y: Complement C5a regulates interleukine-17 by affecting the crosstalk between DCs and gammadelta T cells in CLP-induced sepsis. Eur J Immunol 40: 1079-1088, 2010.
124. Henry T, Kirimanjeswara GS, Ruby T, Jones JW, Peng K, Perret M, Ho L, Sauer JD, Iwakura Y, Metzger DW, et al.: Type I IFN signaling constrains IL-17A/F secretion by {gamma}{delta} T cells during bacterial infections. J Immunol 184:3755-3767, 2010.
125. Tschop J, Martignoni A, Goetzman HS, Choi LG, Wang Q, Noel JG, Ogle CK, Pritts TA, Johannigman JA, Lentsch AB, et al.: Gammadelta T cells mitigate the organ injury and mortality of sepsis. J Leukoc Biol 83:581-588, 2008.
126. Chung CS, Watkins L, Funches A, Lomas-Neira J, Cioffi WG, Ayala A: Deficiency of gammadelta T lymphocytes contributes to mortality and immunosuppression in sepsis. Am J Physiol Regul Integr Comp Physiol 291:R1338YR1343, 2006.
127. Enoh VT, Lin SH, Lin CY, Toliver-Kinsky T, Murphey ED, Varma TK Sherwood ER: Mice depleted of alphabeta but not gammadelta T cells are resistant to mortality caused by cecal ligation and puncture. Shock 27:507-519, 2007.
128. Kasten KR, Muenzer JT, Caldwell CC: Neutrophils are significant producers of IL-10 during sepsis. Biochem Biophys Res Commun 393:28-31, 2010.
129. Gordon S: Alternative activation of macrophages. Nat Rev Immunol 3:23-35, 2003.
130. Meyer CN, Nielsen H: Priming of neutrophil and monocyte activation in human immunodeficiency virus infection. Comparison of granulocyte colony-stimulating factor, granulocyte-macrophage colony-stimulating factor and interferon-gamma. APMIS 104:640-646, 1996.
131. Kapp A, Zeck-Kapp G: Activation of the oxidative metabolism in human polymorphonuclear neutrophilic granulocytes: the role of immuno-modulating cytokines. J Invest Dermatol 95:94-99, 1990.
132. Barth E, Fischer G, Schneider EM, Moldawer LL, Georgieff M, Weiss M: Peaks of endogenous G-CSF serum concentrations are followed by an increase in respiratory burst activity of granulocytes in patients with septic shock. Cytokine 17:275-284, 2002.
133. Netea MG, Van Der Meer JW, Van Deuren M, Kullberg BJ: Proinflammatory cytokines and sepsis syndrome: not enough, or too much of a good thing? Trends Immunol 24:254-258, 2003.
134. Cheung DL, Hart PH, Vitti GF, Whitty GA, Hamilton JA: Contrasting effects of interferon-gamma and interleukin-4 on the interleukin-6 activity of stimulated human monocytes. Immunology 71:70-75, 1990.
135. Fossiez F, Djossou O, Chomarat P, Flores-Romo L, Ait-Yahia S, Maat C, Pin JJ, Garrone P, Garcia E, Saeland S, et al.: T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med 183:2593-2603, 1996.