Removal of regulatory T cells prevents secondary chronic infection but increases the mortality of subsequent sub-acute infection in sepsis mice

Oncotarget

Volumn 7, Issue 10, 2016, Pages 10962-10975

  Huo, Ruichao ^a   Wang, Lili ^a   Wang, Xiaoya ^a   Zhao, Yong ^b   Wang, Yi ^b   Zhao, Xiaomin ^a   Chang, Lingling ^a   Liu, Shan Lu ^c   Tong, Dewen ^a   Zhang, Hai ^b   Huang, Yong ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c University of Missouri   (United States)

Author keywords

Immune response; Immunity; Immunology and microbiology section; Immunosuppression; Immunotherapeutic approach; Lymphocyte; Secondary infection; Sepsis

Indexed keywords

ANTIBODY; CD25 ANTIBODY; GAMMA INTERFERON; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL SURVIVAL; CECAL LIGATION AND PUNCTURE-INDUCED SEPSIS; CELL COUNT; CELL EXPANSION; CELL LOSS; CONTROLLED STUDY; DOWN REGULATION; IMMUNOSUPPRESSIVE TREATMENT; INFECTION; INFECTION PREVENTION; LIPOPOLYSACCHARIDE-INDUCED ENDOTOXEMIA; LYMPHOCYTE; MALE; MORTALITY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PERITONITIS; REGULATORY T LYMPHOCYTE; SEPSIS; SURVIVAL RATE; ANIMAL; C57BL MOUSE; CHRONIC DISEASE; HUMAN; IMMUNOLOGY; PATHOLOGY; PROCEDURES; SURVIVAL ANALYSIS;

ANIMALS; CHRONIC DISEASE; HUMANS; IMMUNOSUPPRESSION; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; SEPSIS; SURVIVAL ANALYSIS; T-LYMPHOCYTES, REGULATORY;

EID: 84961989607     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7682     Document Type: Article

References (37)

1. Hoyert DL, Xu J. Deaths: preliminary data for 2011. Natl Vital Stat Rep. 2012; 61: 1-51.
2. Bosmann M, Ward PA. The inflammatory response in sepsis. Trends Immunol. 2013; 34: 129-136.
3. Bone RC. Sir Isaac Newton, sepsis, SIRS, and CARS. Crit Care Med. 1996; 24: 1125-1128.
4. Rivers E, Nguyen B, Havstad S, Ressler J, Muzzin A, Knoblich B, Peterson E, and Tomlanovich M. Early goal-directed therapy in the treatment of severe sepsis and septic shock. N Engl J Med. 2001; 345: 1368-1377.
5. O'Neill R, Morales J and Jule M. Early goal-directed therapy (EGDT) for severe sepsis/septic shock: which components of treatment are more difficult to implement in a community-based emergency department. J Emerg Med. 2012; 42: 503-510.
6. Knaus WA, Harrell FE, Jr., LaBrecque JF, Wagner DP, Pribble JP, Draper EA, Fisher CJ, and Soll L. Use of predicted risk of mortality to evaluate the efficacy of anticytokine therapy in sepsis. The rhIL-1ra Phase III Sepsis Syndrome Study Group. Crit Care Med. 1996; 24: 46-56.
7. Xiao H, Siddiqui J and Remick DG. Mechanisms of mortality in early and late sepsis. Infect Immun. 2006; 74: 5227-5235.
8. Osuchowski MF, Welch K, Yang H, Siddiqui J and Remick DG. Chronic sepsis mortality characterized by an individualized inflammatory response. J Immunol. 2007; 179: 623-630.
9. Tinsley KW, Grayson MH, Swanson PE, Drewry AM, Chang KC, Karl IE, and Hotchkiss RS. Sepsis induces apoptosis and profound depletion of splenic interdigitating and follicular dendritic cells. J Immunol. 2003; 171: 909-914.
10. Otto GP, Sossdorf M, Claus RA, Rodel J, Menge K, Reinhart K, Bauer M, and Riedemann NC. The late phase of sepsis is characterized by an increased microbiological burden and death rate. Crit Care. 2011; 15: R183.
11. Hotchkiss RS, Coopersmith CM, McDunn JE and Ferguson TA. The sepsis seesaw: tilting toward immunosuppression. Nat Med. 2009; 15: 496-497.
12. Keynan Y, Card CM, McLaren PJ, Dawood MR, Kasper K and Fowke KR. The role of regulatory T cells in chronic and acute viral infections. Clin Infect Dis. 2008; 46: 1046-1052.
13. Venet F, Huang X, Chung CS, Chen Y and Ayala A. Plasmacytoid dendritic cells control lung inflammation and monocyte recruitment in indirect acute lung injury in mice. Am J Pathol. 2010; 176: 764-773.
14. Wisnoski N, Chung CS, Chen Y, Huang X and Ayala A. The contribution of CD4+ CD25+ T-regulatory-cells to immune suppression in sepsis. Shock. 2007; 27: 251-257.
15. Hotchkiss RS, Nicholson DW. Apoptosis and caspases regulate death and inflammation in sepsis. Nat Rev Immunol. 2006; 6: 813-822.
16. Inoue S, Unsinger J, Davis CG, Muenzer JT, Ferguson TA, Chang K, Osborne DF, Clark AT, Coopersmith CM, McDunn JE. IL-15 prevents apoptosis, reverses innate and adaptive immune dysfunction, and improves survival in sepsis. J Immunol. 2010; 184: 1401-1409.
17. Okeke EB, Okwor I, Mou Z, Jia P and Uzonna JE. CD4+CD25+ regulatory T cells attenuate lipopolysaccharide-induced systemic inflammatory responses and promotes survival in murine Escherichia coli infection. Shock. 2013; 40: 65-73.
18. Souza-Fonseca-Guimaraes F, Parlato M, Fitting C, Cavaillon JM and Adib-Conquy M. NK cell tolerance to TLR agonists mediated by regulatory T cells after polymicrobial sepsis. J Immunol. 2012; 188: 5850-5858.
19. Setiady YY, Coccia JA and Park PU. In vivo depletion of CD4+FOXP3+ Treg cells by the PC61 anti-CD25 monoclonal antibody is mediated by FcgammaRIII+ phagocytes. Eur J Immunol. 2010; 40: 780-786.
20. Gautier EL, Huby T, Saint-Charles F, Ouzilleau B, Chapman MJ and Lesnik P. Enhanced dendritic cell survival attenuates lipopolysaccharide-induced immunosuppression and increases resistance to lethal endotoxic shock. J Immunol. 2008; 180: 6941-6946.
21. Okeke EB, Okwor I and Uzonna JE. Regulatory T cells restrain CD4+ T cells from causing unregulated immune activation and hypersensitivity to lipopolysaccharide challenge. J Immunol. 2014; 193: 655-662.
22. Ayala A, Herdon CD, Lehman DL, Ayala CA and Chaudry IH. Differential induction of apoptosis in lymphoid tissues during sepsis: variation in onset, frequency, and the nature of the mediators. Blood. 1996; 87: 4261-4275.
23. Le Tulzo Y, Pangault C, Gacouin A, Guilloux V, Tribut O, Amiot L, Tattevin P, Thomas R, Fauchet R, and Drenou B. Early circulating lymphocyte apoptosis in human septic shock is associated with poor outcome. Shock. 2002; 18: 487-494.
24. Menges T, Engel J, Welters I, Wagner RM, Little S, Ruwoldt R, Wollbrueck M, and Hempelmann G. Changes in blood lymphocyte populations after multiple trauma: association with posttraumatic complications. Crit Care Med. 1999; 27: 733-740.
25. Nascimento DC, Alves-Filho JC, Sonego F, Fukada SY, Pereira MS, Benjamim C, Zamboni DS, Silva JS, and Cunha FQ. Role of regulatory T cells in long-term immune dysfunction associated with severe sepsis. Crit Care Med. 2010; 38: 1718-1725.
26. Cavassani KA, Carson WFt, Moreira AP, Wen H, Schaller MA, Ishii M, Lindell DM, Dou Y, Lukacs NW, Keshamouni VG, Hogaboam CM, Kunkel SL. The post sepsis-induced expansion and enhanced function of regulatory T cells create an environment to potentiate tumor growth. Blood. 2010; 115: 4403-4411.
27. Tatura R, Zeschnigk M, Hansen W, Steinmann J, Vidigal PG, Hutzler M, Pastille E, Westendorf AM, Buer J, and Kehrmann J. Relevance of Foxp3(+) regulatory T cells for early and late phases of murine sepsis. Immunology. 2015; 146: 144-156.
28. Ono S, Kimura A, Hiraki S, Takahata R, Tsujimoto H, Kinoshita M, Miyazaki H, Yamamoto J, Hase K, and Saitoh D. Removal of increased circulating CD4+CD25+Foxp3+ regulatory T cells in patients with septic shock using hemoperfusion with polymyxin B-immobilized fibers. Surgery. 2013; 153: 262-271.
29. Deans KJ, Haley M, Natanson C, Eichacker PQ and Minneci PC. Novel therapies for sepsis: a review. J Trauma. 2005; 58: 867-874.
30. Lehmann C, Sharawi N, Al-Banna N, Corbett N, Kuethe JW and Caldwell CC. Novel approaches to the development of anti-sepsis drugs. Expert Opin Drug Discov. 2014; 9: 523-531.
31. Souza-Fonseca-Guimaraes F, Parlato M, Fitting C, Cavaillon JM and Adib-Conquy M. NK cell tolerance to TLR agonists mediated by regulatory T cells after polymicrobial sepsis. J Immunol. 2012; 188: 5850-5858.
32. Baker CC, Chaudry IH, Gaines HO and Baue AE. Evaluation of factors affecting mortality rate after sepsis in a murine cecal ligation and puncture model. Surgery. 1983; 94: 331-335.
33. Muenzer JT, Davis CG, Chang K, Schmidt RE, Dunne WM, Coopersmith CM, and Hotchkiss RS. Characterization and modulation of the immunosuppressive phase of sepsis. Infect Immun. 2010; 78: 1582-1592.
34. Osuchowski MF, Craciun F, Weixelbaumer KM, Duffy ER and Remick DG. Sepsis chronically in MARS: systemic cytokine responses are always mixed regardless of the outcome, magnitude, or phase of sepsis. J Immunol. 2010; 189: 4648-4656.
35. Osuchowski MF, Welch K, Siddiqui J and Remick DG. Circulating cytokine/inhibitor profiles reshape the understanding of the SIRS/CARS continuum in sepsis and predict mortality. J Immunol. 2006; 177: 1967-1974.
36. Huang Y, Lei Y, Zhang H, Zhang M and Dayton A. Interleukin-12 treatment down-regulates STAT4 and induces apoptosis with increasing ROS production in human natural killer cells. J Leukoc Biol. 2011; 90: 87-97.
37. Huang Y, Lei Y, Zhang H, Hou L, Zhang M and Dayton AI. MicroRNA regulation of STAT4 protein expression: rapid and sensitive modulation of IL-12 signaling in human natural killer cells. Blood. 2011; 118: 6793-6802.