Intestine-specific overexpression of IL-10 improves survival in polymicrobial sepsis

Shock

Volumn 29, Issue 4, 2008, Pages 483-489

  Rajan, Saju ^a   Vyas, Dinesh ^a   Clark, Andrew T ^a   Woolsey, Cheryl A ^a   Clark, Jessica A ^a   Hotchkiss, Richard S ^a   Buchman, Timothy G ^a   Coopersmith, Craig M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Cecal ligation and puncture; Cytokine; Gut; IL 6; MCP 1; Mortality; Splenocyte

Indexed keywords

INTERLEUKIN 10;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; INTESTINE EPITHELIUM; INTESTINE MUCOSA PERMEABILITY; LEUKOCYTE COUNT; LUNG LAVAGE; MORTALITY; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PROTEIN EXPRESSION; SEPSIS; SURVIVAL; SURVIVAL RATE;

ANIMALS; APOPTOSIS; ENDOTOXINS; GENOTYPE; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-10; INTERLEUKIN-6; INTESTINES; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SEPSIS; SPLEEN; SURVIVAL ANALYSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 40949147457     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/SHK.0b013e31815bbb26     Document Type: Article

References (35)

1. Marchant A, Alegre ML, Hakim A, Pierard G, Marecaux G, Friedman G, De GD, Kahn RJ, Vincent JL, Goldman M: Clinical and biological significance of interleukin-10 plasma levels in patients with septic shock. J Clin Immunol 15:266-273, 1995.
2. Scumpia PO, Moldawer LL: Biology of interleukin-10 and its regulatory roles in sepsis syndromes. Crit Care Med 33:S468-S471, 2005.
3. Pajkrt D, van der PT, Levi M, Cutler DL, Affrime MB, van den EA, ten Cate JW, van Deventer SJ: Interleukin-10 inhibits activation of coagulation and fibrinolysis during human endotoxemia. Blood 89:2701-2705, 1997.
4. van der PT, Marchant A, Buurman WA, Berman L, Keogh CV, Lazarus DD, Nguyen L, Goldman M, Moldawer LL, Lowry SF: Endogenous IL-10 protects mice from death during septic peritonitis. J Immunol 155:5397-5401, 1995.
5. Remick DG, Garg SJ, Newcomb DE, Wollenberg G, Huie TK, Bolgos GL: Exogenous interleukin-10 fails to decrease the mortality or morbidity of sepsis. Crit Care Med 26:895-904, 1998.
6. Murphey ED, Sherwood ER: Bacterial clearance and mortality are not improved by a combination of IL-10 neutralization and IFN-gamma administration in a murine model of post-CLP immunosuppression. Shock 26:417-424, 2006.
7. Donnelly SC, Strieter RM, Reid PT, Kunkel SL, Burdick MD, Armstrong I, Mackenzie A, Haslett C: The association between mortality rates and decreased concentrations of interleukin-10 and interleukin-1 receptor antagonist in the lung fluids of patients with the adult respiratory distress syndrome. Ann Intern Med 125:191-196, 1996.
8. McAuliffe PF, Murday ME, Efron PA, Scumpia PO, Ungaro R, Abouhamze A, Tannahill CL, Hutchins B, LaFace D, Moldawer LL: Dose-dependent improvements in outcome with adenoviral expression of interleukin-10 in a murine model of multisystem organ failure. Gene Ther 13:276-282, 2006.
9. Oberholzer C, Oberholzer A, Bahjat FR, Minter RM, Tannahill CL, Abouhamze A, LaFace D, Hutchins B, Clare-Salzler MJ, Moldawer LL: Targeted adenovirus-induced expression of IL-10 decreases thymic apoptosis and improves survival in murine sepsis. Proc Natl Acad Sci U S A 98:11503-11508, 2001.
10. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W: Interleukin-10- deficient mice develop chronic enterocolitis. Cell 75:263-274, 1993.
11. Berg DJ, Davidson N, Kuhn R, Muller W, Menon S, Holland G, Thompson-Snipes L, Leach MW, Rennick D: Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J Clin Invest 98:1010-1020, 1996.
12. De WH, Elewaut D, Turovskaya O, Huflejt M, Shimeld C, Hagenbaugh A, Binder S, Takahashi I, Kronenberg M, Cheroutre H: Regulation of mucosal immune responses by recombinant interleukin 10 produced by intestinal epithelial cells in mice. Gastroenterology 122:1829-1841, 2002.
13. Hassoun HT, Kone BC, Mercer DW, Moody FG, Weisbrodt NW, Moore FA: Post-injury multiple organ failure: the role of the gut. Shock 15:1-10, 2001.
14. Carrico CJ, Meakins JL, Marshall JC, Fry D, Maier RV: Multiple-organ-failure syndrome. The gastrointestinal tract: the "motor" of MOF. Arch Surg 121:196-208, 1986.
15. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR: Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 29:1303-1310, 2001.
16. Baker CC, Chaudry IH, Gaines HO, Baue AE: Evaluation of factors affecting mortality rate after sepsis in a murine cecal ligation and puncture model. Surgery 94:331-335, 1983.
17. Husain KD, Stromberg PE, Woolsey CA, Turnbull IR, Dunne WM, Javadi P, Buchman TG, Karl IE, Hotchkiss RS, Coopersmith CM: Mechanisms of decreased intestinal epithelial proliferation and increased apoptosis in murine acute lung injury. Crit Care Med 33:2350-2357, 2005.
18. Turnbull IR, Buchman TG, Javadi P, Woolsey CA, Hotchkiss RS, Karl IE, Coopersmith CM: Age disproportionately increases sepsis-induced apoptosis in the spleen and gut epithelium. Shock 22:364-368, 2004.
19. Yang R, Han X, Uchiyama T, Watkins SK, Yaguchi A, Delude RL, Fink MP: IL-6 is essential for development of gut barrier dysfunction after hemorrhagic shock and resuscitation in mice. Am J Physiol Gastrointest Liver Physiol 285:G621-G629, 2003.
20. Sims CA, Wattanasirichaigoon S, Menconi MJ, Ajami AM, Fink MP: Ringer's ethyl pyruvate solution ameliorates ischemia/reperfusion-induced intestinal mucosal injury in rats. Crit Care Med 29:1513-1518, 2001.
21. Todd D, Singh AJ, Greiner DL, Mordes JP, Rossini AA, Bortell R: A new isolation method for rat intraepithelial lymphocytes. J Immunol Methods 224:111-127, 1999.
22. Hotchkiss RS, Chang KC, Swanson PE, Tinsley KW, Hui JJ, Klender P, Xanthoudakis S, Roy S, Black C, Grimm E, et al.: Caspase inhibitors improve survival in sepsis: a critical role of the lymphocyte. Nat Immunol 1:496-501, 2000.
23. Deitch EA, Xu D, Kaise VL: Role of the gut in the development of injury- and shock induced SIRS and MODS: the gut-lymph hypothesis, a review. Front Biosci 11:520-528, 2006.
24. Andrejko KM, Chen J, Deutschman CS: Intrahepatic STAT-3 activation and acute phase gene expression predict outcome after CLP sepsis in the rat. Am J Physiol 275:G1423-G1429, 1998.
25. Remick DG, Bolgos GR, Siddiqui J, Shin J, Nemzek JA: Six at six: interleukin-6 measured 6 h after the initiation of sepsis predicts mortality over 3 days. Shock 17:463-467, 2002.
26. Xiao H, Remick DG: Correction of perioperative hypothermia decreases experimental sepsis mortality by modulating the inflammatory response. Crit Care Med 33:161-167, 2005.
27. Vianna RC, Gomes RN, Bozza FA, Amancio RT, Bozza PT, David CM, Castro-Faria-Neto HC: Antibiotic treatment in a murine model of sepsis: impact on cytokines and endotoxin release. Shock 21:115-120, 2004.
28. Vyas D, Javadi P, Dipasco PJ, Buchman TG, Hotchkiss RS, Coopersmith CM: Early antibiotic administration but not antibody therapy directed against IL-6 improves survival in septic mice predicted to die on basis of high IL-6 levels. Am J Physiol Regul Integr Comp Physiol 289:R1048-R1053, 2005.
29. Deutschman CS, Cereda M, Ochroch EA, Raj NR: Sepsis-induced cholestasis, steatosis, hepatocellular injury, and impaired hepatocellular regeneration are enhanced in interleukin-6 -/- mice. Crit Care Med 34:2613-2620, 2006.
30. Zhou P, Streutker C, Borojevic R, Wang Y, Croitoru K: IL-10 modulates intestinal damage and epithelial cell apoptosis in T cell-mediated enteropathy. Am J Physiol Gastrointest Liver Physiol 287:G599-G604, 2004.
31. Coopersmith CM, Stromberg PE, Dunne WM, Davis CG, Amiot DM, Buchman TG, Karl IE, Hotchkiss RS: Inhibition of intestinal epithelial apoptosis and survival in a murine model of pneumonia-induced sepsis. JAMA 287:1716-1721, 2002.
32. Coopersmith CM, Chang KC, Swanson PE, Tinsley KW, Stromberg PE, Buchman TG, Karl IE, Hotchkiss RS: Overexpression of Bcl-2 in the intestinal epithelium improves survival in septic mice. Crit Care Med 30:195-201, 2002.
33. Madsen KL, Malfair D, Gray D, Doyle JS, Jewell LD, Fedorak RN: Interleukin-10 gene-deficient mice develop a primary intestinal permeability defect in response to enteric microflora. Inflamm Bowel Dis 5:262-270, 1999.
34. Deitch EA: Animal models of sepsis and shock: a review and lessons learned. Shock 9:1-11, 1998.
35. Marshall JC: Neutrophils in the pathogenesis of sepsis. Crit Care Med 33:S502-S505, 2005.