Inhibition of IκB kinase reduces the multiple organ dysfunction caused by sepsis in the mouse

DMM Disease Models and Mechanisms

Volumn 6, Issue 4, 2013, Pages 1031-1042

  Coldewey, Sina M ^a,b   Rogazzo, Mara ^c   Collino, Massimo ^c   Patel, Nimesh S A ^a   Thiemermann, Christoph ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; CREATININE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; I KAPPA B; I KAPPA B ALPHA; I KAPPA B KINASE 16; I KAPPA B KINASE INHIBITOR; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; MYELOPEROXIDASE; PEPTIDOGLYCAN; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CECAL LIGATION AND PUNCTURE; ECHOCARDIOGRAPHY; ENZYME INHIBITION; HEART DISEASE; IN VIVO STUDY; KIDNEY DYSFUNCTION; LIVER CELL DAMAGE; MALE; MOUSE; MULTIPLE ORGAN FAILURE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROCEDURES; SEPSIS;

ANIMALS; CECUM; HEART FUNCTION TESTS; I-KAPPA B KINASE; I-KAPPA B PROTEINS; KIDNEY; LIGATION; LIPOPOLYSACCHARIDES; LIVER; MALE; MICE; MICE, INBRED C57BL; MULTIPLE ORGAN FAILURE; MYOCARDIUM; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PEPTIDOGLYCAN; PNEUMONIA; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PUNCTURES; SEPSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA;

BACTERIA (MICROORGANISMS); MUS;

EID: 84880010135     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.012435     Document Type: Article

References (57)

1. Abdelrahman, M., Sivarajah, A. and Thiemermann, C. (2005). Beneficial effects of PPAR-gamma ligands in ischemia-reperfusion injury, inflammation and shock. Cardiovasc. Res. 65, 772-781. (Pubitemid 40249723)
2. Abraham, E. and Singer, M. (2007). Mechanisms of sepsis-induced organ dysfunction. Crit. Care Med. 35, 2408-2416. (Pubitemid 47476242)
3. Angus, D. C., Linde-Zwirble, W. T., Lidicker, J., Clermont, G., Carcillo, J. and Pinsky, M. R. (2001). Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29, 1303-1310. (Pubitemid 32641789)
4. Arnalich, F., Garcia-Palomero, E., López, J., Jiménez, M., Madero, R., Renart, J., Vázquez, J. J. and Montiel, C. (2000). Predictive value of nuclear factor kappaB activity and plasma cytokine levels in patients with sepsis. Infect. Immun. 68, 1942-1945. (Pubitemid 30164821)
5. Bakker, J., Grover, R., McLuckie, A., Holzapfel, L., Andersson, J., Lodato, R., Watson, D., Grossman, S., Donaldson, J., Takala, J.; Glaxo Wellcome International Septic Shock Study Group (2004). Administration of the nitric oxide synthase inhibitor NG-methyl-L-arginine hydrochloride (546C88) by intravenous infusion for up to 72 hours can promote the resolution of shock in patients with severe sepsis: results of a randomized, double-blind, placebo-controlled multicenter study (study no. 144-002). Crit. Care Med. 32, 1-12. (Pubitemid 38125557)
6. Barone, F. C., Hillegass, L. M., Price, W. J., White, R. F., Lee, E. V., Feuerstein, G. Z., Sarau, H. M., Clark, R. K. and Griswold, D. E. (1991). Polymorphonuclear leukocyte infiltration into cerebral focal ischemic tissue: myeloperoxidase activity assay and histologic verification. J. Neurosci. Res. 29, 336-345.
7. Barth, E., Radermacher, P., Thiemermann, C., Weber, S., Georgieff, M. and Albuszies, G. (2006). Role of inducible nitric oxide synthase in the reduced responsiveness of the myocardium to catecholamines in a hyperdynamic, murine model of septic shock. Crit. Care Med. 34, 307-313. (Pubitemid 43145605)
8. Bone, R. C., Balk, R. A., Cerra, F. B., Dellinger, R. P., Fein, A. M., Knaus, W. A., Schein, R. M., Sibbald, W. J.; The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine (1992). Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Chest 101, 1644-1655.
9. Brady, A. J., Poole-Wilson, P. A., Harding, S. E. and Warren, J. B. (1992). Nitric oxide production within cardiac myocytes reduces their contractility in endotoxemia. Am. J. Physiol. 263, H1963-H1966. (Pubitemid 23030755)
10. Cantley, L. C. (2002). The phosphoinositide 3-kinase pathway. Science 296, 1655-1657.
11. Celes, M. R., Prado, C. M. and Rossi, M. A. (2013). Sepsis: going to the heart of the matter. Pathobiology 80, 70-86.
12. Chen, G., Cao, P. and Goeddel, D. V. (2002). TNF-induced recruitment and activation of the IKK complex require Cdc37 and Hsp90. Mol. Cell 9, 401-410. (Pubitemid 34195564)
13. Coldewey, S. M., Khan, A. I., Kapoor, A., Collino, M., Rogazzo, M., Brines, M., Cerami, A., Hall, P., Sheaff, M., Kieswich, J. E. et al. (2013). Erythropoietin attenuates acute kidney dysfunction in murine experimental sepsis by activation of the β-common receptor. Kidney Int. [Epub ahead of print] doi: 10.1038/ki.2013.118.
14. Collino, M., Aragno, M., Mastrocola, R., Benetti, E., Gallicchio, M., Dianzani, C., Danni, O., Thiemermann, C. and Fantozzi, R. (2006). Oxidative stress and inflammatory response evoked by transient cerebral ischemia/reperfusion: effects of the PPAR-alpha agonist WY14643. Free Radic. Biol. Med. 41, 579-589. (Pubitemid 44080506)
15. Collino, M., Castiglia, S., Manoni, M., Salsini, L., Chini, J., Masini, E. and Fantozzi, R. (2009). Effects of a semi-synthetic N-,O-sulfated glycosaminoglycan K5 polysaccharide derivative in a rat model of cerebral ischaemia/reperfusion injury. Thromb. Haemost. 102, 837-845.
16. De Gaudio, A. R., Rinaldi, S., Chelazzi, C. and Borracci, T. (2009). Pathophysiology of sepsis in the elderly: clinical impact and therapeutic considerations. Curr. Drug Targets 10, 60-70.
17. de Souza, A. C., Volpini, R. A., Shimizu, M. H., Sanches, T. R., Camara, N. O., Semedo, P., Rodrigues, C. E., Seguro, A. C. and Andrade, L. (2012). Erythropoietin prevents sepsis-related acute kidney injury in rats by inhibiting NF-κB and upregulating endothelial nitric oxide synthase. Am. J. Physiol. Renal Physiol. 302, F1045-F1054.
18. Dombrovskiy, V. Y., Martin, A. A., Sunderram, J. and Paz, H. L. (2007). Rapid increase in hospitalization and mortality rates for severe sepsis in the United States: a trend analysis from 1993 to 2003. Crit. Care Med. 35, 1244-1250. (Pubitemid 46642649)
19. Dugo, L., Collin, M., Cuzzocrea, S. and Thiemermann, C. (2004). 15d-prostaglandin J2 reduces multiple organ failure caused by wall-fragment of Gram-positive and Gram-negative bacteria. Eur. J. Pharmacol. 498, 295-301. (Pubitemid 39208092)
20. Dugo, L., Collin, M., Allen, D. A., Patel, N. S., Bauer, I., Mervaala, E. M., Louhelainen, M., Foster, S. J., Yaqoob, M. M. and Thiemermann, C. (2005). GSK- 3beta inhibitors attenuate the organ injury/dysfunction caused by endotoxemia in the rat. Crit. Care Med. 33, 1903-1912. (Pubitemid 41306508)
21. Dugo, L., Collin, M., Allen, D. A., Murch, O., Foster, S. J., Yaqoob, M. M. and Thiemermann, C. (2006). Insulin reduces the multiple organ injury and dysfunction caused by coadministration of lipopolysaccharide and peptidoglycan independently of blood glucose: role of glycogen synthase kinase-3beta inhibition. Crit. Care Med. 34, 1489-1496.
22. Fleming, I. and Busse, R. (2003). Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284, R1-R12. (Pubitemid 36008649)
23. Flynn, A., Chokkalingam Mani, B. and Mather, P. J. (2010). Sepsis-induced cardiomyopathy: a review of pathophysiologic mechanisms. Heart Fail. Rev. 15, 605-611.
24. Fontana, J., Fulton, D., Chen, Y., Fairchild, T. A., McCabe, T. J., Fujita, N., Tsuruo, T. and Sessa, W. C. (2002). Domain mapping studies reveal that the M domain of hsp90 serves as a molecular scaffold to regulate Akt-dependent phosphorylation of endothelial nitric oxide synthase and NO release. Circ. Res. 90, 866-873. (Pubitemid 34633878)
25. Girard, T. D., Opal, S. M. and Ely, E. W. (2005). Insights into severe sepsis in older patients: from epidemiology to evidence-based management. Clin. Infect. Dis. 40, 719-727. (Pubitemid 40381348)
26. Jacobs, M. D. and Harrison, S. C. (1998). Structure of an IkappaBalpha/NF-kappaB complex. Cell 95, 749-758.
27. Kapoor, A., Shintani, Y., Collino, M., Osuchowski, M. F., Busch, D., Patel, N. S., Sepodes, B., Castiglia, S., Fantozzi, R., Bishop-Bailey, D. et al. (2010). Protective role of peroxisome proliferator-activated receptor-β/δ in septic shock. Am. J. Respir. Crit. Care Med. 182, 1506-1515.
28. Kengatharan, K. M., De Kimpe, S. J. and Thiemermann, C. (1996). Role of nitric oxide in the circulatory failure and organ injury in a rodent model of gram-positive shock. Br. J. Pharmacol. 119, 1411-1421. (Pubitemid 26402019)
29. Khan, R., Kirschenbaum, L. A., LaRow, C., Berna, G., Griffin, K. and Astiz, M. E. (2010). Augmentation of platelet and endothelial cell eNOS activity decreases sepsis-related neutrophil-endothelial cell interactions. Shock 33, 242-246.
30. Khan, A. I., Coldewey, S. M., Patel, N. S., Rogazzo, M., Collino, M., Yaqoob, M. M., Radermacher, P., Kapoor, A. and Thiemermann, C. (2013). Erythropoietin attenuates cardiac dysfunction in experimental sepsis in mice via activation of the β-common receptor. Dis. Model. Mech. [Epub ahead of print] doi:10.1242/dmm.011908.
31. Laubach, V. E., Shesely, E. G., Smithies, O. and Sherman, P. A. (1995). Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc. Natl. Acad. Sci. USA 92, 10688-10692.
32. Laubach, V. E., Foley, P. L., Shockey, K. S., Tribble, C. G. and Kron, I. L. (1998). Protective roles of nitric oxide and testosterone in endotoxemia: evidence from NOS-2-deficient mice. Am. J. Physiol. 275, H2211-H2218.
33. Li, Q., Van Antwerp, D., Mercurio, F., Lee, K. F. and Verma, I. M. (1999a). Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science 284, 321-325. (Pubitemid 129523450)
34. Li, Z. W., Chu, W., Hu, Y., Delhase, M., Deerinck, T., Ellisman, M., Johnson, R. and Karin, M. (1999b). The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. J. Exp. Med. 189, 1839-1845. (Pubitemid 29272700)
35. López, A., Lorente, J. A., Steingrub, J., Bakker, J., McLuckie, A., Willatts, S., Brockway, M., Anzueto, A., Holzapfel, L., Breen, D. et al. (2004). Multiple-center, randomized, placebo-controlled, double-blind study of the nitric oxide synthase inhibitor 546C88: effect on survival in patients with septic shock. Crit. Care Med. 32, 21-30. (Pubitemid 38125559)
36. MacMicking, J. D., Nathan, C., Hom, G., Chartrain, N., Fletcher, D. S., Trumbauer, M., Stevens, K., Xie, Q. W., Sokol, K., Hutchinson, N. et al. (1995). Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81, 641-650.
37. Mao, K., Chen, S., Chen, M., Ma, Y., Wang, Y., Huang, B., He, Z., Zeng, Y., Hu, Y., Sun, S. et al. (2013). Nitric oxide suppresses NLRP3 inflammasome activation and protects against LPS-induced septic shock. Cell Res. 23, 201-212.
38. Mohan, S., Konopinski, R., Yan, B., Centonze, V. E. and Natarajan, M. (2009). High glucose-induced IKK-Hsp-90 interaction contributes to endothelial dysfunction. Am. J. Physiol. Cell Physiol. 296, C182-C192.
39. Moynagh, P. N. (2005). The NF-kappaB pathway. J. Cell Sci. 118, 4589-4592.
40. Rivers, E., Nguyen, B., Havstad, S., Ressler, J., Muzzin, A., Knoblich, B., Peterson, E., Tomlanovich, M.; Early Goal-Directed Therapy Collaborative Group (2001). Early goal-directed therapy in the treatment of severe sepsis and septic shock. N. Engl. J. Med. 345, 1368-1377.
41. Rudiger, A. and Singer, M. (2007). Mechanisms of sepsis-induced cardiac dysfunction. Crit. Care Med. 35, 1599-1608. (Pubitemid 46809326)
42. Ruetten, H. and Thiemermann, C. (1997). Effect of calpain inhibitor I, an inhibitor of the proteolysis of I kappa B, on the circulatory failure and multiple organ dysfunction caused by endotoxin in the rat. Br. J. Pharmacol. 121, 695-704. (Pubitemid 27260772)
43. Sen, R. and Baltimore, D. (1986). Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 46, 705-716. (Pubitemid 16020062)
44. Senftleben, U. and Karin, M. (2002). The IKK/NF-kappa B pathway. Crit. Care Med. 30 Suppl., S18-S26.
45. Szabó, C., Mitchell, J. A., Thiemermann, C. and Vane, J. R. (1993). Nitric oxide-mediated hyporeactivity to noradrenaline precedes the induction of nitric oxide synthase in endotoxin shock. Br. J. Pharmacol. 108, 786-792. (Pubitemid 23067954)
46. Szabó, C., Southan, G. J. and Thiemermann, C. (1994). Beneficial effects and improved survival in rodent models of septic shock with S-methylisothiourea sulfate, a potent and selective inhibitor of inducible nitric oxide synthase. Proc. Natl. Acad. Sci. USA 91, 12472-12476.
47. Thiemermann, C. and Vane, J. (1990). Inhibition of nitric oxide synthesis reduces the hypotension induced by bacterial lipopolysaccharides in the rat in vivo. Eur. J. Pharmacol. 182, 591-595. (Pubitemid 20260783)
48. Tyml, K. (2011). Critical role for oxidative stress, platelets, and coagulation in capillary blood flow impairment in sepsis. Microcirculation 18, 152-162.
49. Waelchli, R., Bollbuck, B., Bruns, C., Buhl, T., Eder, J., Feifel, R., Hersperger, R., Janser, P., Revesz, L., Zerwes, H. G. et al. (2006). Design and preparation of 2-benzamido-pyrimidines as inhibitors of IKK. Bioorg. Med. Chem. Lett. 16, 108-112. (Pubitemid 41625653)
50. Wang, H. E., Shapiro, N. I., Angus, D. C. and Yealy, D. M. (2007). National estimates of severe sepsis in United States emergency departments. Crit. Care Med. 35, 1928-1936. (Pubitemid 47220368)
51. Watson, D., Grover, R., Anzueto, A., Lorente, J., Smithies, M., Bellomo, R., Guntupalli, K., Grossman, S., Donaldson, J., Le Gall, J. R.; Glaxo Wellcome International Septic Shock Study Group (2004). Cardiovascular effects of the nitric oxide synthase inhibitor NG-methyl-L-arginine hydrochloride (546C88) in patients with septic shock: results of a randomized, double-blind, placebo-controlled multicenter study (study no. 144-002). Crit. Care Med. 32, 13-20. (Pubitemid 38125558)
52. Wei, X. Q., Charles, I. G., Smith, A., Ure, J., Feng, G. J., Huang, F. P., Xu, D., Muller, W., Moncada, S. and Liew, F. Y. (1995). Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375, 408-411.
53. Wichterman, K. A., Baue, A. E. and Chaudry, I. H. (1980). Sepsis and septic shock - a review of laboratory models and a proposal. J. Surg. Res. 29, 189-201. (Pubitemid 10039498)
54. Wray, G. M., Foster, S. J., Hinds, C. J. and Thiemermann, C. (2001). A cell wall component from pathogenic and non-pathogenic gram-positive bacteria (peptidoglycan) synergises with endotoxin to cause the release of tumour necrosis factor-alpha, nitric oxide production, shock, and multiple organ injury/dysfunction in the rat. Shock 15, 135-142. (Pubitemid 33598175)
55. Yang, K. Y., Arcaroli, J. J. and Abraham, E. (2003). Early alterations in neutrophil activation are associated with outcome in acute lung injury. Am. J. Respir. Crit. Care Med. 167, 1567-1574. (Pubitemid 37363369)
56. Zingarelli, B. and Cook, J. A. (2005). Peroxisome proliferator-activated receptor-gamma is a new therapeutic target in sepsis and inflammation. Shock 23, 393-399. (Pubitemid 40571660)
57. Zingarelli, B., Piraino, G., Hake, P. W., O'Connor, M., Denenberg, A., Fan, H. and Cook, J. A. (2010). Peroxisome proliferator-activated receptor delta regulates inflammation via NF-kappaB signaling in polymicrobial sepsis. Am. J. Pathol. 177, 1834-1847. Forschungsgemeinschaft Forschungsgemeinschaft