Isoflurane activates intestinal sphingosine kinase to protect against bilateral nephrectomy-induced liver and intestine dysfunction

American Journal of Physiology - Renal Physiology

Volumn 300, Issue 1, 2011, Pages

  Kim, Minjae ^a   Park, Sang Won ^a   Kim, Mihwa ^a   D'Agati, Vivette D ^a   Lee, H Thomas ^a  

^a Columbia University ^*  (United States)

Author keywords

Acute kidney injury; Acute renal failure; Apoptosis; Inflammation; Necrosis; Sphingosine 1 phosphate

Indexed keywords

ISOFLURANE; MESSENGER RNA; PENTOBARBITAL; PHOSPHOTRANSFERASE INHIBITOR; SPHINGOSINE KINASE 1;

ACUTE KIDNEY FAILURE; ANESTHESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL VACUOLE; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME ACTIVITY; GENE EXPRESSION; HISTOPATHOLOGY; INTESTINE CRYPT; INTESTINE FUNCTION; INTESTINE INJURY; INTESTINE NECROSIS; KIDNEY INJURY; LIVER CELL; MALE; MOUSE; NEPHRECTOMY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

EID: 78651269911     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00467.2010     Document Type: Article

References (59)

1. Abelha FJ, Botelho M, Fernandes V, Barros H. Determinants of postoperative acute kidney injury. Crit Care 13: R79, 2009.
2. Allende ML, Sasaki T, Kawai H, Olivera A, Mi Y, van Echten-Deckert G, Hajdu R, Rosenbach M, Keohane CA, Mandala S, Spiegel S, Proia RL. Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J Biol Chem 279: 52487-52492, 2004. (Pubitemid 39656625)
3. Antkowiak B. How do general anaesthetics work? Naturwissenschaften 88: 201-213, 2001. (Pubitemid 32588419)
4. Atarashi K, Nishimura J, Shima T, Umesaki Y, Yamamoto M, Onoue M, Yagita H, Ishii N, Evans R, Honda K, Takeda K. ATP drives lamina propria T(H)17 cell differentiation. Nature 455: 808-812, 2008.
5. Awad AS, Ye H, Huang L, Li L, Foss FW Jr, Macdonald TL, Lynch KR, Okusa MD. Selective sphingosine 1-phosphate 1 receptor activation reduces ischemia-reperfusion injury in mouse kidney. Am J Physiol Renal Physiol 290: F1516-F1524, 2006. (Pubitemid 43830779)
6. Bonventre JV, Zuk A. Ischemic acute renal failure: an inflammatory disease? Kidney Int 66: 480-485, 2004.
7. Cousins MJ, Skowronski G, Plummer JL. Anaesthesia and the kidney. Anaesth Intensive Care 11: 292-320, 1983.
8. Di A, Kawamura T, Gao XP, Tang H, Berdyshev E, Vogel SM, Zhao YY, Sharma T, Bachmaier K, Xu J, Malik AB. A novel function of sphingosine kinase 1 suppression of JNK activity in preventing inflammation and injury. J Biol Chem 285: 15848-15857, 2010.
9. Donnahoo KK, Shames BD, Harken AH, Meldrum DR. Review article: the role of tumor necrosis factor in renal ischemia-reperfusion injury. J Urol 162: 196-203, 1999. (Pubitemid 29420927)
10. Elapavaluru S, Kellum JA. Why do patients die of acute kidney injury? Acta Clin Belg Suppl: 326-331, 2007.
11. French KJ, Schrecengost RS, Lee BD, Zhuang Y, Smith SN, Eberly JL, Yun JK, Smith CD. Discovery and evaluation of inhibitors of human sphingosine kinase. Cancer Res 63: 5962-5969, 2003.
12. French KJ, Upson JJ, Keller SN, Zhuang Y, Yun JK, Smith CD. Antitumor activity of sphingosine kinase inhibitors. J Pharmacol Exp Ther 318: 596-603, 2006.
13. Fuller TF, Hoff U, Kong L, Naether M, Wagner P, Nieminen-Kelha M, Nolting J, Luft FC, Hegner B, Dragun D. Cytoprotective actions of FTY720 modulate severe preservation reperfusion injury in rat renal transplants. Transplantation 89: 402-408, 2010.
14. Fyrst H, Saba JD. An update on sphingosine-1-phosphate and other sphingolipid mediators. Nat Chem Biol 6: 489-497, 2010.
15. Golab F, Kadkhodaee M, Zahmatkesh M, Hedayati M, Arab H, Schuster R, Zahedi K, Lentsch AB, Soleimani M. Ischemic and nonischemic acute kidney injury cause hepatic damage. Kidney Int 75: 783-792, 2009.
16. Greenspon J, Li R, Xiao L, Rao JN, Marasa BS, Strauch ED, Wang JY, Turner DJ. Sphingosine-1-phosphate protects intestinal epithelial cells from apoptosis through the Akt signaling pathway. Dig Dis Sci 54: 499-510, 2009.
17. Hait NC, Oskeritzian CA, Paugh SW, Milstien S, Spiegel S. Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim Biophys Acta 1758: 2016-2026, 2006. (Pubitemid 44879368)
18. Hassoun HT, Grigoryev DN, Lie ML, Liu M, Cheadle C, Tuder RM, Rabb H. Ischemic acute kidney injury induces a distant organ functional and genomic response distinguishable from bilateral nephrectomy. Am J Physiol Renal Physiol 293: F30-F40, 2007.
19. Hoke TS, Douglas IS, Klein CL, He Z, Fang W, Thurman JM, Tao Y, Dursun B, Voelkel NF, Edelstein CL, Faubel S. Acute renal failure after bilateral nephrectomy is associated with cytokine-mediated pulmonary injury. J Am Soc Nephrol 18: 155-164, 2007. (Pubitemid 46070147)
20. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, Cua DJ, Littman DR. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133, 2006.
21. Jamnicki-Abegg M, Weihrauch D, Pagel PS, Kersten JR, Bosnjak ZJ, Warltier DC, Bienengraeber MW. Isoflurane inhibits cardiac myocyte apoptosis during oxidative and inflammatory stress by activating Akt and enhancing Bcl-2 expression. Anesthesiology 103: 1006-1014, 2005.
22. Jin X, Zimmers TA, Zhang Z, Pierce RH, Koniaris LG. Interleukin-6 is an important in vivo inhibitor of intestinal epithelial cell death in mice. Gut 59: 186-196, 2010.
23. Jin ZQ, Karliner JS, Vessey DA. Ischaemic postconditioning protects isolated mouse hearts against ischaemia/reperfusion injury via sphingosine kinase isoform-1 activation. Cardiovasc Res 79: 134-140, 2008.
24. Jones DR, Lee HT. Perioperative renal protection. Best Pract Res Clin Anaesthesiol 22: 193-208, 2008.
25. Joo JD, Kim M, D'Agati VD, Lee HT. Ischemic preconditioning provides both acute and delayed protection against renal ischemia and reperfusion injury in mice. J Am Soc Nephrol 17: 3115-3123, 2006. (Pubitemid 44707771)
26. Kaudel CP, Frink M, van Griensven M, Schmiddem U, Probst C, Bergmann S, Krettek C, Klempnauer J, Winkler M. FTY720 application following isolated warm liver ischemia improves long-term survival and organ protection in a mouse model. Transplant Proc 39: 493-498, 2007.
27. Kelly KJ. Distant effects of experimental renal ischemia/reperfusion injury. J Am Soc Nephrol 14: 1549-1558, 2003. (Pubitemid 36687056)
28. Kim do J, Park SH, Sheen MR, Jeon US, Kim SW, Koh ES, Woo SK. Comparison of experimental lung injury from acute renal failure with injury due to sepsis. Respiration 73: 815-824, 2006.
29. Kim M, Kim M, Park SW, Pitson SM, Lee HT. Isoflurane protects human kidney proximal tubule cells against necrosis via sphingosine kinase and sphingosine-1-phosphate generation. Am J Nephrol 31: 353-362, 2010.
30. Kim M, Kim N, Kim M, D'Agati VD, Emala CW Sr, Lee HT. Isoflurane mediates protection from renal ischemia-reperfusion injury via sphingosine kinase and sphingosine-1-phosphate-dependent pathways. Am J Physiol Renal Physiol 293: F1827-F1835, 2007.
31. Klein CL, Hoke TS, Fang WF, Altmann CJ, Douglas IS, Faubel S. Interleukin-6 mediates lung injury following ischemic acute kidney injury or bilateral nephrectomy. Kidney Int 74: 901-909, 2008.
32. Lee HT, Kim M, Kim M, Kim N, Billings FT IV, D'Agati VD, Emala CW Sr. Isoflurane protects against renal ischemia and reperfusion injury and modulates leukocyte infiltration in mice. Am J Physiol Renal Physiol 293: F713-F722, 2007. (Pubitemid 47403341)
33. Lee HT, Ota-Setlik A, Fu Y, Nasr SH, Emala CW. Differential protective effects of volatile anesthetics against renal ischemia-reperfusion injury in vivo. Anesthesiology 101: 1313-1324, 2004.
34. Lee HT, Park SW, Kim M, D'Agati VD. Acute kidney injury after hepatic ischemia and reperfusion injury in mice. Lab Invest 89: 196-208, 2009.
35. Lien YH, Yong KC, Cho C, Igarashi S, Lai LW. S1P(1)-selective agonist, SEW2871, ameliorates ischemic acute renal failure. Kidney Int 69: 1601-1608, 2006.
36. Liu M, Liang Y, Chigurupati S, Lathia JD, Pletnikov M, Sun Z, Crow M, Ross CA, Mattson MP, Rabb H. Acute kidney injury leads to inflammation and functional changes in the brain. J Am Soc Nephrol 19: 1360-1370, 2008.
37. Lochhead KM, Zager RA. Fluorinated anesthetic exposure "activates" the renal cortical sphingomyelinase cascade. Kidney Int 54: 373-381, 1998.
38. Maceyka M, Payne SG, Milstien S, Spiegel S. Sphingosine kinase, sphingosine-1-phosphate, and apoptosis. Biochim Biophys Acta 1585: 193-201, 2002.
39. Maines LW, Fitzpatrick LR, Green CL, Zhuang Y, Smith CD. Efficacy of a novel sphingosine kinase inhibitor in experimental Crohn's disease. Inflammopharmacology 18: 73-85, 2010.
40. Mehta RL, Pascual MT, Gruta CG, Zhuang S, Chertow GM. Refining predictive models in critically ill patients with acute renal failure. J Am Soc Nephrol 13: 1350-1357, 2002.
41. Mu J, Xie K, Hou L, Peng D, Shang L, Ji G, Li J, Lu Y, Xiong L. Subanesthetic dose of isoflurane protects against zymosan-induced generalized inflammation and its associated acute lung injury in mice. Shock 34: 183-189, 2010.
42. Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, Karin M. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 317: 121-124, 2007. (Pubitemid 47056470)
43. Okazaki M, Kreisel F, Richardson SB, Kreisel D, Krupnick AS, Patterson GA, Gelman AE. Sphingosine 1-phosphate inhibits ischemia reperfusion injury following experimental lung transplantation. Am J Transplant 7: 751-758, 2007.
44. Olivera A, Eisner C, Kitamura Y, Dillahunt S, Allende L, Tuymetova G, Watford W, Meylan F, Diesner SC, Li L, Schnermann J, Proia RL, Rivera J. Sphingosine kinase 1 and sphingosine-1-phosphate receptor 2 are vital to recovery from anaphylactic shock in mice. J Clin Invest 120: 1429-1440, 2010.
45. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6: 1133-1141, 2005.
46. Park SW, Chen SWC, Kim M, Brown KM, Kolls JK, D'Agati VD, Lee HT. Cytokines induce small intestine and liver injury after renal ischemia or nephrectomy. Lab Invest. Epub ahead of print.
47. Park SW, Kim M, Chen S, Brown K, Kolls J, Lee HT. Paneth cell activation after acute kidney injury causes liver and intestine injury and systemic inflammation in mice (Abstract). J Immunol 184: 35.39, 2010.
48. Park SW, Kim M, Chen SW, D'Agati VD, Lee HT. Sphinganine-1-phosphate attenuates both hepatic and renal injury induced by hepatic ischemia and reperfusion in mice. Shock 33: 31-42, 2010.
49. Pecoits-Filho R, Heimburger O, Barany P, Suliman M, Fehrman-Ekholm I, Lindholm B, Stenvinkel P. Associations between circulating inflammatory markers and residual renal function in CRF patients. Am J Kidney Dis 41: 1212-1218, 2003.
50. Schmidt R, Tritschler E, Hoetzel A, Loop T, Humar M, Halverscheid L, Geiger KK, Pannen BH. Heme oxygenase-1 induction by the clinically used anesthetic isoflurane protects rat livers from ischemia/reperfusion injury. Ann Surg 245: 931-942, 2007.
51. Snider AJ, Kawamori T, Bradshaw SG, Orr KA, Gilkeson GS, Hannun YA, Obeid LM. A role for sphingosine kinase 1 in dextran sulfate sodium-induced colitis. FASEB J 23: 143-152, 2009.
52. Soukup J, Scharff K, Kubosch K, Pohl C, Bomplitz M, Kompardt J. State of the art: sedation concepts with volatile anesthetics in critically ill patients. J Crit Care 24: 535-544, 2009.
53. Spiegel S, Milstien S. Sphingosine 1-phosphate, a key cell signaling molecule. J Biol Chem 277: 25851-25854, 2002.
54. Steurer M, Schlapfer M, Z'Graggen BR, Booy C, Reyes L, Spahn DR, Beck-Schimmer B. The volatile anaesthetic sevoflurane attenuates lipopolysaccharide-induced injury in alveolar macrophages. Clin Exp Immunol 155: 224-230, 2009.
55. Sugito K, Inoue M, Ikeda T, Hagiwara N, Koshinaga T, Kusafuka T. Effect of FTY720 and ex vivo graft irradiation in rat small bowel transplantation: apoptosis of crypt cells and lymphocytes. Transplant Proc 39: 3432-3435, 2007.
56. Takahashi N, Vanlaere I, de Rycke R, Cauwels A, Joosten LA, Lubberts E, van den Berg WB, Libert C. IL-17 produced by Paneth cells drives TNF-induced shock. J Exp Med 205: 1755-1761, 2008.
57. Vessey DA, Kelley M, Karliner JS. A rapid radioassay for sphingosine kinase. Anal Biochem 337: 136-142, 2005.
58. Yang S, Koo DJ, Chaudry IH, Wang P. The important role of the gut in initiating the hyperdynamic response during early sepsis. J Surg Res 89: 31-37, 2000. (Pubitemid 30127439)
59. Zhou Y, Lekic T, Fathali N, Ostrowski RP, Martin RD, Tang J, Zhang JH. Isoflurane posttreatment reduces neonatal hypoxic-ischemic brain injury in rats by the sphingosine-1-phosphate/phosphatidylinositol-3-kinase/Akt pathway. Stroke 41: 1521-1527, 2010.