Inhibition of IKKβ in enterocytes exacerbates sepsis-induced intestinal injury and worsens mortality

Critical Care Medicine

Volumn 41, Issue 10, 2013, Pages

  Dominguez, Jessica A ^a   Samocha, Alexandr J ^b   Liang, Zhe ^c   Burd, Eileen M ^c   Farris, Alton B ^c   Coopersmith, Craig M ^c  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Gut; NF Kb; Permeability; Sepsis; Tumor necrosis factor

Indexed keywords

CLAUDIN 2; GAMMA INTERFERON; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; OCCLUDIN; PROTEIN ZO1;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BACTERIAL LOAD; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE EXACERBATION; ENZYME INHIBITION; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; INTESTINE INJURY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SEPSIS; WILD TYPE;

ANIMALS; APOPTOSIS; CELL MEMBRANE PERMEABILITY; ENTEROCYTES; I-KAPPA B KINASE; INTESTINAL MUCOSA; MICE; MODELS, ANIMAL; PROSPECTIVE STUDIES; RANDOM ALLOCATION; SEPSIS; TUMOR NECROSIS FACTORS;

EID: 84884907987     PISSN: 00903493     EISSN: 15300293     Source Type: Journal    
DOI: 10.1097/CCM.0b013e31828a44ed     Document Type: Article

References (61)

1. Angus DC, Linde-Zwirble WT, Lidicker J, et al: Epidemiology of severe sepsis in the United States: Analysis of incidence, outcome, and associated costs of care. Crit Care Med 2001; 29:1303-1310 (Pubitemid 32641789)
2. Martin GS, Mannino DM, Eaton S, et al: The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 2003; 348:1546-1554 (Pubitemid 36437931)
3. Clark JA, Coopersmith CM: Intestinal crosstalk: a new paradigm for understanding the gut as the "motor" of critical illness. Shock 2007; 28:384-393 (Pubitemid 47421846)
4. Hassoun HT, Kone BC, Mercer DW, et al: Post-injury multiple organ failure: The role of the gut. Shock 2001; 15:1-10 (Pubitemid 33598153)
5. Carrico CJ, Meakins JL, Marshall JC, et al: Multiple-organ-failure syndrome. Arch Surg 1986; 121:196-208
6. Clark JA, Clark AT, Hotchkiss RS, et al: Epidermal growth factor treatment decreases mortality and is associated with improved gut integrity in sepsis. Shock 2008; 30:36-42
7. 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 1997; 7:247-253 (Pubitemid 127654275)
8. Coopersmith CM, Stromberg PE, Dunne WM, et al: Inhibition of intestinal epithelial apoptosis and survival in a murine model of pneumoniainduced sepsis. JAMA 2002; 287:1716-1721 (Pubitemid 34289225)
9. Hotchkiss RS, Swanson PE, Freeman BD, et al: Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit Care Med 1999; 27:1230-1251 (Pubitemid 29379358)
10. Stromberg PE, Woolsey CA, Clark AT, et al: CD4+ lymphocytes control gut epithelial apoptosis and mediate survival in sepsis. FASEB J 2009; 23:1817-1825
11. Coopersmith CM, Chang KC, Swanson PE, et al: Overexpression of Bcl-2 in the intestinal epithelium improves survival in septic mice. Crit Care Med 2002; 30:195-201 (Pubitemid 34112196)
12. Dominguez JA, Vithayathil PJ, Khailova L, et al: Epidermal growth factor improves survival and prevents intestinal injury in a murine model of pseudomonas aeruginosa pneumonia. Shock 2011; 36:381-389
13. Vyas D, Robertson CM, Stromberg PE, et al: Epithelial apoptosis in mechanistically distinct methods of injury in the murine small intestine. Histol Histopathol 2007; 22:623-630 (Pubitemid 46647274)
14. Clark JA, Gan H, Samocha AJ, et al: Enterocyte-specific epidermal growth factor prevents barrier dysfunction and improves mortality in murine peritonitis. Am J Physiol Gastrointest Liver Physiol 2009; 297:G471-G479
15. De-Souza DA, Greene LJ: Intestinal permeability and systemic infections in critically ill patients: Effect of glutamine. Crit Care Med 2005; 33:1125-1135 (Pubitemid 40638191)
16. Neal MD, Leaphart C, Levy R, et al: Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier. J Immunol 2006; 176:3070-3079
17. Fink MP: Intestinal epithelial hyperpermeability: Update on the pathogenesis of gut mucosal barrier dysfunction in critical illness. Curr Opin Crit Care 2003; 9:143-151 (Pubitemid 36408134)
18. Mainous MR, Ertel W, Chaudry IH, et al: The gut: A cytokine-generating organ in systemic inflammation? Shock 1995; 4:193-199
19. Hayden MS, Ghosh S: Shared principles in NF-kappaB signaling. Cell 2008; 132:344-362
20. Ghosh S, Karin M: Missing pieces in the NF-kappaB puzzle. Cell 2002; 109(Suppl):S81-S96
21. Spehlmann ME, Eckmann L: Nuclear factor-kappa B in intestinal protection and destruction. Curr Opin Gastroenterol 2009; 25:92-99
22. Eckmann L, Nebelsiek T, Fingerle AA, et al: Opposing functions of IKKbeta during acute and chronic intestinal inflammation. Proc Natl Acad Sci USA 2008; 105:15058-15063
23. Hayden MS, Ghosh S: Signaling to NF-kappaB. Genes Dev 2004; 18:2195-2224
24. Karin M, Lin A: NF-kappaB at the crossroads of life and death. Nat Immunol 2002; 3:221-227
25. Li Q, Van Antwerp D, Mercurio F, et al: Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science 1999; 284:321-325 (Pubitemid 129523450)
26. Wullaert A, Bonnet MC, Pasparakis M: NF-κB in the regulation of epithelial homeostasis and inflammation. Cell Res 2011; 21:146-158
27. Lawrance IC, Wu F, Leite AZ, et al: A murine model of chronic inflammation-induced intestinal fibrosis down-regulated by antisense NF-kappa B. Gastroenterology 2003; 125:1750-1761 (Pubitemid 37500440)
28. MacMaster JF, Dambach DM, Lee DB, et al: An inhibitor of IkappaB kinase, BMS-345541, blocks endothelial cell adhesion molecule expression and reduces the severity of dextran sulfate sodiuminduced colitis in mice. Inflamm Res 2003; 52:508-511 (Pubitemid 38058225)
29. Shibata W, Maeda S, Hikiba Y, et al: Cutting edge: The IkappaB kinase (IKK) inhibitor, NEMO-binding domain peptide, blocks inflammatory injury in murine colitis. J Immunol 2007; 179:2681-2685
30. Davé SH, Tilstra JS, Matsuoka K, et al: Amelioration of chronic murine colitis by peptide-mediated transduction of the IkappaB kinase inhibitor NEMO binding domain peptide. J Immunol 2007; 179:7852-7859
31. Greten FR, Eckmann L, Greten TF, et al: IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004; 118:285-296 (Pubitemid 39061110)
32. Chen LW, Chen PH, Chang WJ, et al: IKappaB-kinase/nuclear factorkappaB signaling prevents thermal injury-induced gut damage by inhibiting c-Jun NH2-terminal kinase activation. Crit Care Med 2007; 35:1332-1340
33. Chae S, Eckmann L, Miyamoto Y, et al: Epithelial cell I kappa B-kinase beta has an important protective role in Clostridium difficile toxin A-induced mucosal injury. J Immunol 2006; 177:1214-1220 (Pubitemid 44036626)
34. Chen LW, Egan L, Li ZW, et al: The two faces of IKK and NF-kappaB inhibition: Prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion. Nat Med 2003; 9:575-581 (Pubitemid 36597104)
35. Baker CC, Chaudry IH, Gaines HO, et al: Evaluation of factors affecting mortality rate after sepsis in a murine cecal ligation and puncture model. Surgery 1983; 94:331-335 (Pubitemid 13043132)
36. Fox AC, Robertson CM, Belt B, et al: Cancer causes increased mortality and is associated with altered apoptosis in murine sepsis. Crit Care Med 2010; 38:886-893
37. Danielsson A, Hellers G, Lyrenäs E, et al: A controlled randomized trial of budesonide versus prednisolone retention enemas in active distal ulcerative colitis. Scand J Gastroenterol 1987; 22:987-992 (Pubitemid 17152840)
38. D'Haens GR, Geboes K, Peeters M, et al: Early lesions of recurrent Crohn's disease caused by infusion of intestinal contents in excluded ileum. Gastroenterology 1998; 114:262-267 (Pubitemid 28093532)
39. Wells CL, Hess DJ, Erlandsen SL: Impact of the indigenous flora in animal models of shock and sepsis. Shock 2004; 22:562-568 (Pubitemid 39576585)
40. Robertson CM, Perrone EE, McConnell KW, et al: Neutrophil depletion causes a fatal defect in murine pulmonary Staphylococcus aureus clearance. J Surg Res 2008; 150:278-285
41. Zingarelli B, Sheehan M, Wong HR: Nuclear factor-kappaB as a therapeutic target in critical care medicine. Crit Care Med 2003; 31(1 Suppl):S105-S111 (Pubitemid 36143484)
42. Li X, Su J, Cui X, et al: Can we predict the effects of NF-kappaB inhibition in sepsis? Studies with parthenolide and ethyl pyruvate. Expert Opin Investig Drugs 2009; 18:1047-1060
43. Wheeler DS, Zingarelli B, Wheeler WJ, et al: Novel pharmacologic approaches to the management of sepsis: Targeting the host inflammatory response. Recent Pat Inflamm Allergy Drug Discov 2009; 3:96-112
44. Uwe S: Anti-inflammatory interventions of NF-kappaB signaling: Potential applications and risks. Biochem Pharmacol 2008; 75:1567-1579
45. Egan LJ, Eckmann L, Greten FR, et al: IkappaB-kinasebeta-dependent NF-kappaB activation provides radioprotection to the intestinal epithelium. Proc Natl Acad Sci USA 2004; 101:2452-2457 (Pubitemid 38269332)
46. Chin AC, Flynn AN, Fedwick JP, et al: The role of caspase-3 in lipopolysaccharide- mediated disruption of intestinal epithelial tight junctions. Can J Physiol Pharmacol 2006; 84:1043-1050
47. Sun Z, Wang X, Deng X, et al: The influence of intestinal ischemia and reperfusion on bidirectional intestinal barrier permeability, cellular membrane integrity, proteinase inhibitors, and cell death in rats. Shock 1998; 10:203-212 (Pubitemid 128464311)
48. Zeissig S, Bürgel N, Günzel D, et al: Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut 2007; 56:61-72 (Pubitemid 46044890)
49. Heller F, Florian P, Bojarski C, et al: Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 2005; 129:550-564 (Pubitemid 41096643)
50. Hotchkiss RS, Opal S: Immunotherapy for sepsis-A new approach against an ancient foe. N Engl J Med 2010; 363:87-89
51. Hotchkiss RS, Karl IE: The pathophysiology and treatment of sepsis. N Engl J Med 2003; 348:138-150 (Pubitemid 36056721)
52. McConnell KW, McDunn JE, Clark AT, et al: Streptococcus pneumoniae and Pseudomonas aeruginosa pneumonia induce distinct host responses. Crit Care Med 2010; 38:223-241
53. Hotchkiss RS, Coopersmith CM, McDunn JE, et al: The sepsis seesaw: Tilting toward immunosuppression. Nat Med 2009; 15:496-497
54. Osuchowski MF, Welch K, Siddiqui J, et al: Circulating cytokine/inhibitor profiles reshape the understanding of the SIRS/CARS continuum in sepsis and predict mortality. J Immunol 2006; 177:1967-1974
55. Courtine E, P?ne F, Cagnard N, et al: Critical role of cRel subunit of NF-?B in sepsis survival. Infect Immun 2011; 79:1848-1854
56. Papa S, Zazzeroni F, Bubici C, et al: Gadd45 beta mediates the NF-kappa B suppression of JNK signalling by targeting MKK7/ JNKK2. Nat Cell Biol 2004; 6:146-153 (Pubitemid 38425714)
57. Mankertz J, Amasheh M, Krug SM, et al: TNFalpha up-regulates claudin- 2 expression in epithelial HT-29/B6 cells via phosphatidylinositol- 3-kinase signaling. Cell Tissue Res 2009; 336:67-77
58. Qiu P, Cui X, Barochia A, et al: The evolving experience with therapeutic TNF inhibition in sepsis: Considering the potential influence of risk of death. Expert Opin Investig Drugs 2011; 20:1555-1564
59. Lorente JA, Marshall JC: Neutralization of tumor necrosis factor in preclinical models of sepsis. Shock 2005; 24 Suppl 1:107-119
60. Riché FC, Cholley BP, Panis YH, et al: Inflammatory cytokine response in patients with septic shock secondary to generalized peritonitis. Crit Care Med 2000; 28:433-437 (Pubitemid 30120885)
61. Singleton KD, Wischmeyer PE: Distance of cecum ligated influences mortality, tumor necrosis factor-alpha and interleukin-6 expression following cecal ligation and puncture in the rat. Eur Surg Res 2003; 35:486-491 (Pubitemid 37346753)