Renal effects of treatment with a TLR4 inhibitor in conscious septic sheep

Critical Care

Volumn 18, Issue 5, 2014, Pages

  Fenhammar, Johan ^a   Rundgren, Mats ^b   Hultenby, Kjell ^b   Forestier, Jakob ^a   Taavo, Micael ^c   Kenne, Ellinor ^a,b   Weitzberg, Eddie ^b   Eriksson, Stefan ^b   Ozenci, Volkan ^a   Wernerson, Annika ^b   Frithiof, Robert ^b,c  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; N ACETYL BETA GLUCOSAMINIDASE; RESATORVID; TOLL LIKE RECEPTOR 4; BIOLOGICAL MARKER; ETHYL 6-(N-(2-CHLORO-4-FLUOROPHENYL)SULFAMOYL)CYCLOHEX-1-ENE-1-CARBOXYLATE; SULFONAMIDE;

ACUTE KIDNEY FAILURE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SWELLING; CONTINUOUS INFUSION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CREATININE CLEARANCE; ESCHERICHIA COLI; HYPERLACTATEMIA; KIDNEY BLOOD FLOW; KIDNEY CORTEX; KIDNEY MEDULLA; KIDNEY PERFUSION; KIDNEY VASCULAR RESISTANCE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHARMACOLOGICAL BLOCKING; RENAL PROTECTION; SEPSIS; SHEEP; URINE VOLUME; ACUTE KIDNEY INJURY; ANIMAL; BLOOD; COMPLICATION; DISEASE MODEL; DOMESTIC SHEEP; DRUG EFFECTS; ESCHERICHIA COLI INFECTIONS; FEMALE; GLOMERULUS FILTRATION RATE; KIDNEY; KIDNEY CIRCULATION; MICROBIOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; URINE;

ACUTE KIDNEY INJURY; ANIMALS; BIOMARKERS; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; GLOMERULAR FILTRATION RATE; KIDNEY; RENAL CIRCULATION; SEPSIS; SHEEP, DOMESTIC; SULFONAMIDES;

EID: 84907932362     PISSN: 13648535     EISSN: 1466609X     Source Type: Journal    
DOI: 10.1186/s13054-014-0488-y     Document Type: Article

References (51)

1. Murugan R, Kellum JA. Acute kidney injury: what's the prognosis?. Nat Rev Nephrol 2011, 7:209-217. 10.1038/nrneph.2011.13, 21343898.
2. Schrier RW, Wang W. Acute renal failure and sepsis. N Engl J Med 2004, 351:159-169. 10.1056/NEJMra032401, 15247356.
3. Fenhammar J, Rundgren M, Forestier J, Kalman S, Eriksson S, Frithiof R. Toll-like receptor 4 inhibitor TAK-242 attenuates acute kidney injury in endotoxemic sheep. Anesthesiology 2011, 114:1130-1137. 10.1097/ALN.0b013e31820b8b44, 21394006.
4. Frithiof R, Soehnlein O, Eriksson S, Fenhammar J, Hjelmqvist H, Lindbom L, Rundgren M. The effects of isoflurane anesthesia and mechanical ventilation on renal function during endotoxemia. Acta Anaesthesiol Scand 2011, 55:401-410. 10.1111/j.1399-6576.2011.02406.x, 21391922.
5. Ishikawa K, Bellomo R, May CN. The impact of intrarenal nitric oxide synthase inhibition on renal blood flow and function in mild and severe hyperdynamic sepsis. Crit Care Med 2011, 39:770-776. 10.1097/CCM.0b013e318206c1fb, 21169816.
6. Lerolle N, Nochy D, Guerot E, Bruneval P, Fagon JY, Diehl JL, Hill G. Histopathology of septic shock induced acute kidney injury: apoptosis and leukocytic infiltration. Intensive Care Med 2010, 36:471-478. 10.1007/s00134-009-1723-x, 19924395.
7. Medzhitov R, Preston-Hurlburt P, Janeway CA. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 1997, 388:394-397. 10.1038/41131, 9237759.
8. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 1999, 162:3749-3752. 10201887.
9. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282:2085-2088. 10.1126/science.282.5396.2085, 9851930.
10. Qureshi ST, Lariviere L, Leveque G, Clermont S, Moore KJ, Gros P, Malo D. Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4). J Exp Med 1999, 189:615-625. 10.1084/jem.189.4.615, 9989976.
11. Kawai T, Akira S. TLR signaling. Semin Immunol 2007, 19:24-32. 10.1016/j.smim.2006.12.004, 17275323.
12. Daubeuf B, Mathison J, Spiller S, Hugues S, Herren S, Ferlin W, Kosco-Vilbois M, Wagner H, Kirschning CJ, Ulevitch R, Elson G. TLR4/MD-2 monoclonal antibody therapy affords protection in experimental models of septic shock. J Immunol 2007, 179:6107-6114. 10.4049/jimmunol.179.9.6107, 17947685.
13. Goldfarb RD, Ortegel JW, Parrillo JE, Zanotti-Cavazzoni S, Casey LC, Dellinger RP. TAKEDA-143242 increased survival via reduced cytokines in porcine peritonitis. J Surg Res 2011, 166:e165-e173. 10.1016/j.jss.2010.09.031, 21236445.
14. Kuno M, Nemoto K, Ninomiya N, Inagaki E, Kubota M, Matsumoto T, Yokota H. The novel selective toll-like receptor 4 signal transduction inhibitor tak-242 prevents endotoxaemia in conscious Guinea-pigs. Clin Exp Pharmacol Physiol 2009, 36:589-593. 10.1111/j.1440-1681.2008.05121.x, 19673945.
15. Roger T, Froidevaux C, Le Roy D, Reymond MK, Chanson AL, Mauri D, Burns K, Riederer BM, Akira S, Calandra T. Protection from lethal gram-negative bacterial sepsis by targeting Toll-like receptor 4. Proc Natl Acad Sci U S A 2009, 106:2348-2352. 10.1073/pnas.0808146106, 19181857.
16. Sha T, Sunamoto M, Kitazaki T, Sato J, Ii M, Iizawa Y. Therapeutic effects of TAK-242, a novel selective Toll-like receptor 4 signal transduction inhibitor, in mouse endotoxin shock model. Eur J Pharmacol 2007, 571:231-239. 10.1016/j.ejphar.2007.06.027, 17632100.
17. Sha T, Iizawa Y, Ii M. Combination of imipenem and TAK-242, a Toll-like receptor 4 signal transduction inhibitor, improves survival in a murine model of polymicrobial sepsis. Shock 2011, 35:205-209. 10.1097/SHK.0b013e3181f48942, 20720515.
18. Tidswell M, Tillis W, Larosa SP, Lynn M, Wittek AE, Kao R, Wheeler J, Gogate J, Opal SM. Phase 2 trial of eritoran tetrasodium (E5564), a toll-like receptor 4 antagonist, in patients with severe sepsis. Crit Care Med 2010, 38:72-83. 10.1097/CCM.0b013e3181b07b78, 19661804.
19. Opal SM, Laterre PF, Francois B, LaRosa SP, Angus DC, Mira JP, Wittebole X, Dugernier T, Perrotin D, Tidswell M, Jauregui L, Krell K, Pachl J, Takahashi T, Peckelsen C, Cordasco E, Chang CS, Oeyen S, Aikawa N, Maruyama T, Schein R, Kalil AC, Van Nuffelen M, Lynn M, Rossignol DP, Gogate J, Roberts MB, Wheeler JL, Vincent JL. Effect of eritoran, an antagonist of MD2-TLR4, on mortality in patients with severe sepsis: the ACCESS randomized trial. JAMA 2013, 309:1154-1162. 10.1001/jama.2013.2194, 23512062.
20. Rice TW, Wheeler AP, Bernard GR, Vincent JL, Angus DC, Aikawa N, Demeyer I, Sainati S, Amlot N, Cao C, Ii M, Matsuda H, Mouri K, Cohen J. A randomized, double-blind, placebo-controlled trial of TAK-242 for the treatment of severe sepsis. Crit Care Med 2010, 38:1685-1694. 10.1097/CCM.0b013e3181e7c5c9, 20562702.
21. El Achkar TM, Huang X, Plotkin Z, Sandoval RM, Rhodes GJ, Dagher PC. Sepsis induces changes in the expression and distribution of Toll-like receptor 4 in the rat kidney. Am J Physiol Renal Physiol 2006, 290:F1034-F1043. 10.1152/ajprenal.00414.2005, 16332927.
22. Cunningham PN, Wang Y, Guo R, He G, Quigg RJ. Role of Toll-like receptor 4 in endotoxin-induced acute renal failure. J Immunol 2004, 172:2629-2635. 10.4049/jimmunol.172.4.2629, 14764737.
23. Langenberg C, Wan L, Egi M, May CN, Bellomo R. Renal blood flow in experimental septic acute renal failure. Kidney Int 2006, 69:1996-2002. 10.1038/sj.ki.5000440, 16641923.
24. Doi K, Leelahavanichkul A, Yuen PS, Star RA. Animal models of sepsis and sepsis-induced kidney injury. J Clin Invest 2009, 119:2868-2878. 10.1172/JCI39421, 19805915.
25. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996, 86:973-983. 10.1016/S0092-8674(00)80172-5, 8808632.
26. Moreno G, Errea A, Van Maele L, Roberts R, Léger H, Sirard JC, Benecke A, Rumbo M, Hozbor D. Toll-like receptor 4 orchestrates neutrophil recruitment into airways during the first hours of Bordetella pertussis infection. Microbes Infect 2013, 15:708-718. 10.1016/j.micinf.2013.06.010, 23811096.
27. Matsunaga N, Tsuchimori N, Matsumoto T, Ii M. TAK-242 (resatorvid), a small-molecule inhibitor of Toll-like receptor (TLR) 4 signaling, binds selectively to TLR4 and interferes with interactions between TLR4 and its adaptor molecules. Mol Pharmacol 2011, 79:34-41. 10.1124/mol.110.068064, 20881006.
28. Sharfuddin AA, Molitoris BA. Pathophysiology of ischemic acute kidney injury. Nat Rev Nephrol 2011, 7:189-200. 10.1038/nrneph.2011.16, 21364518.
29. Flynn A, Chokkalingam MB, Mather PJ. Sepsis-induced cardiomyopathy: a review of pathophysiologic mechanisms. Heart Fail Rev 2010, 15:605-611. 10.1007/s10741-010-9176-4, 20571889.
30. Langenberg C, Bagshaw SM, May CN, Bellomo R. The histopathology of septic acute kidney injury: a systematic review. Crit Care 2008, 12:R38. 10.1186/cc6823, 18325092.
31. Chawla LS, Seneff MG, Nelson DR, Williams M, Levy H, Kimmel PL, Macias WL. Elevated plasma concentrations of IL-6 and elevated APACHE II score predict acute kidney injury in patients with severe sepsis. Clin J Am Soc Nephrol 2007, 2:22-30. 10.2215/CJN.02510706, 17699383.
32. May CN, Calzavacca P, Ishikawa K, Langenberg C, Wan L, Ramchandra R, Bellomo R. Novel targets for sepsis-induced kidney injury: the glomerular arterioles and the sympathetic nervous system. Exp Physiol 2012, 97:1168-1177. 10.1113/expphysiol.2011.061804, 22689445.
33. Ishikawa K, Calzavacca P, Bellomo R, Bailey M, May CN. Effect of selective inhibition of renal inducible nitric oxide synthase on renal blood flow and function in experimental hyperdynamic sepsis. Crit Care Med 2012, 40:2368-2375. 10.1097/CCM.0b013e3182514be9, 22622397.
34. Levy B, Gibot S, Franck P, Cravoisy A, Bollaert PE. Relation between muscle Na + K + ATPase activity and raised lactate concentrations in septic shock: a prospective study. Lancet 2005, 365:871-875. 10.1016/S0140-6736(05)71045-X, 15752531.
35. Fredriksson K, Hammarqvist F, Strigard K, Hultenby K, Ljungqvist O, Wernerman J, Rooyackers O. Derangements in mitochondrial metabolism in intercostal and leg muscle of critically ill patients with sepsis-induced multiple organ failure. Am J Physiol Endocrinol Metab 2006, 291:E1044-E1050. 10.1152/ajpendo.00218.2006, 16803854.
36. Wu L, Gokden N, Mayeux PR. Evidence for the role of reactive nitrogen species in polymicrobial sepsis-induced renal peritubular capillary dysfunction and tubular injury. J Am Soc Nephrol 2007, 18:1807-1815. 10.1681/ASN.2006121402, 17494883.
37. Sharfuddin AA, Sandoval RM, Berg DT, McDougal GE, Campos SB, Phillips CL, Jones BE, Gupta A, Grinnell BW, Molitoris BA. Soluble thrombomodulin protects ischemic kidneys. J Am Soc Nephrol 2009, 20:524-534. 10.1681/ASN.2008060593, 19176699.
38. Soehnlein O, Oehmcke S, Ma X, Rothfuchs AG, Frithiof R, van Rooijen N, Mörgelin M, Herwald H, Lindbom L. Neutrophil degranulation mediates severe lung damage triggered by streptococcal M1 protein. Eur Respir J 2008, 32:405-412. 10.1183/09031936.00173207, 18321926.
39. Awad AS, Rouse M, Huang L, Vergis AL, Reutershan J, Cathro HP, Linden J, Okusa MD. Compartmentalization of neutrophils in the kidney and lung following acute ischemic kidney injury. Kidney Int 2009, 75:689-698. 10.1038/ki.2008.648, 19129795.
40. Castoldi A, Braga TT, Correa-Costa M, Aguiar CF, Bassi EJ, Correa-Silva R, Elias RM, Salvador F, Moraes-Vieira PM, Cenedeze MA, Reis MA, Hiyane MI, Pacheco-Silva A, Goncalves GM, Saraiva Camara NO. TLR2, TLR4 and the MYD88 signaling pathway are crucial for neutrophil migration in acute kidney injury induced by sepsis. PLoS One 2012, 7:e37584. 10.1371/journal.pone.0037584, 22655058.
41. Andonegui G, Bonder CS, Green F, Mullaly SC, Zbytnuik L, Raharjo E, Kubes P. Endothelium-derived Toll-like receptor-4 is the key molecule in LPS-induced neutrophil sequestration into lungs. J Clin Invest 2003, 111:1011-1020. 10.1172/JCI16510, 12671050.
42. Chen J, John R, Richardson JA, Shelton JM, Zhou XJ, Wang Y, Wu QQ, Hartono JR, Winterberg PD, Lu CY. Toll-like receptor 4 regulates early endothelial activation during ischemic acute kidney injury. Kidney Int 2011, 79:288-299. 10.1038/ki.2010.381, 20927041.
43. Brown HJ, Lock HR, Wolfs TG, Buurman WA, Sacks SH, Robson MG. Toll-like receptor 4 ligation on intrinsic renal cells contributes to the induction of antibody-mediated glomerulonephritis via CXCL1 and CXCL2. J Am Soc Nephrol 2007, 18:1732-1739. 10.1681/ASN.2006060634, 17460147.
44. Zhang B, Ramesh G, Uematsu S, Akira S, Reeves WB. TLR4 signaling mediates inflammation and tissue injury in nephrotoxicity. J Am Soc Nephrol 2008, 19:923-932. 10.1681/ASN.2007090982, 18256356.
45. Molitoris BA, Sandoval RM. Intravital multiphoton microscopy of dynamic renal processes. Am J Physiol Renal Physiol 2005, 288:F1084-F1089. 10.1152/ajprenal.00473.2004, 15883167.
46. Klausner JM, Paterson IS, Goldman G, Kobzik L, Rodzen C, Lawrence R, Valeri CR, Shepro D, Hechtman HB. Postischemic renal injury is mediated by neutrophils and leukotrienes. Am J Physiol 1989, 256:F794-F802. 2541628.
47. Watts BA, George T, Sherwood ER, Good DW. Basolateral LPS inhibits NHE3 and HCOFormula absorption through TLR4/MyD88-dependent ERK activation in medullary thick ascending limb. Am J Physiol Cell Physiol 2011, 301:C1296-C1306. 10.1152/ajpcell.00237.2011, 21881005.
48. Watts BA, George T, Good DW. Lumen LPS inhibits HCO3(-) absorption in the medullary thick ascending limb through TLR4-PI3K-Akt-mTOR-dependent inhibition of basolateral Na+/H + exchange. Am J Physiol Renal Physiol 2013, 305:F451-F462. 10.1152/ajprenal.00102.2013, 23698118.
49. Watts BA, George T, Sherwood ER, Good DW. A two-hit mechanism for sepsis-induced impairment of renal tubule function. Am J Physiol Renal Physiol 2013, 304:F863-F874. 10.1152/ajprenal.00608.2012, 23324175.
50. Sullivan JC, Wang B, Boesen EI, D'Angelo G, Pollock JS, Pollock DM. Novel use of ultrasound to examine regional blood flow in the mouse kidney. Am J Physiol Renal Physiol 2009, 297:F228-F235. 10.1152/ajprenal.00016.2009, 19420115.
51. Nawaz M, Shah BH. Renal clearance of endogenous creatinine and urea in sheep during summer and winter. Res Vet Sci 1984, 36:220-224. 6718820.