Interleukin-11 protects against renal ischemia and reperfusion injury

American Journal of Physiology - Renal Physiology

Volumn 303, Issue 8, 2012, Pages

  Thomas Lee, H ^a   Park, Sang Won ^a   Kim, Mihwa ^a   Ham, Ahrom ^a   Anderson, Lana J ^b   Brown, Kevin M ^a   D'Agati, Vivette D ^a   Cox, George N ^b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b Bolder BioTechnology Inc   (United States)

Author keywords

Acute kidney injury; Apoptosis; Hypoxia inducible factor 1 ; Inflammation; Necrosis; Sphingosine kinase

Indexed keywords

CREATININE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 11; MACROGOL; RECOMBINANT INTERLEUKIN 11; SPHINGOSINE KINASE 1;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DNA BINDING; ENZYME ACTIVITY; HUMAN; HUMAN CELL; KIDNEY CELL; KIDNEY FUNCTION; KIDNEY ISCHEMIA; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE NECROSIS; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENAL PROTECTION; REPERFUSION INJURY;

EID: 84867733241     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00220.2012     Document Type: Article

References (64)

1. Allende ML, Dreier JL, Mandela S, Proia RL. Expression of the sphingosine 1-phosphate receptor, S1P1, on T-cells controls thymic emigration. J Biol Chem 279: 15396-15401, 2004.
2. Allende ML, Sasaki T, Kawai H, Olivera A, Mi Y, 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.
3. Allende ML, Yamashita T, Proia RL. G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation. Blood 102: 3665-3667, 2003.
4. Bajwa A, Jo SK, Ye H, Huang L, Dondeti KR, Rosin DL, Haase VH, Macdonald TL, Lynch KR, Okusa MD. Activation of sphingosine-1-phosphate 1 receptor in the proximal tubule protects against ischemia-reperfusion injury. J Am Soc Nephrol 21: 955-965, 2010.
5. Bonventre JV, Weinberg JM. Recent advances in the pathophysiology of ischemic acute renal failure. J Am Soc Nephrol 14: 2199-2210, 2003.
6. Bozza M, Bliss JL, Maylor R, Erickson J, Donnelly L, Bouchard P, Dorner AJ, Trepicchio WL. Interleukin-11 reduces T-cell-dependent experimental liver injury in mice. Hepatology 30: 1441-1447, 1999.
7. Chae SS, Proia RL, Hla T. Constitutive expression of the S1P1 receptor in adult tissues. Prostaglandins Other Lipid Mediat 73: 141-150, 2004.
8. Cox GN, Rosendahl MS, Chlipala EA, Smith DJ, Carlson SJ, Doherty DH. A long-acting, mono-PEGylated human growth hormone analog is a potent stimulator of weight gain and bone growth in hypophysectomized rats. Endocrinology 148: 1590-1597, 2007.
9. Du X, Williams DA. Interleukin-11: review of molecular, cell biology, and clinical use. Blood 89: 3897-3908, 1997.
10. Faubel S. Acute kidney injury and multiple organ dysfunction syndrome. Minerva Urol Nefrol 61: 171-188, 2009.
11. Fujio Y, Maeda M, Mohri T, Obana M, Iwakura T, Hayama A, Yamashita T, Nakayama H, Azuma J. Glycoprotein 130 cytokine signal as a therapeutic target against cardiovascular diseases. J Pharmacol Sci 117: 213-222, 2011.
12. Goldman SC, Bracho F, Davenport V, Slack R, Areman E, Shen V, Lenarsky C, Weinthal J, Hughes R, Cairo MS. Feasibility study of IL-11 and granulocyte colony-stimulating factor after myelosuppressive chemotherapy to mobilize peripheral blood stem cells from heavily pre-treated patients. J Pediatr Hematol Oncol 23: 300-305, 2001.
13. Grosfeld JL, Du X, Williams DA. Interleukin-11: its biology and prospects for clinical use. JPEN J Parenter Enteral Nutr 23: S67-S69, 1999.
14. Hait NC, Oskeritzian CA, Paugh SW, Milstien S, Spiegel S. Sphin-gosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim Biophys Acta 1758: 2016-2026, 2006.
15. Hoste EA, Kellum JA. Incidence, classification, and outcomes of acute kidney injury. Contrib Nephrol 156: 32-38, 2007.
16. Hsu HK, Juan SH, Ho PY, Liang YC, Lin CH, Teng CM, Lee WS. YC-1 inhibits proliferation of human vascular endothelial cells through a cyclic GMP-independent pathway. Biochem Pharmacol 66: 263-271, 2003.
17. Ikeda M, Prachasilchai W, Burne-Taney MJ, Rabb H, Yokota-Ikeda N. Ischemic acute tubular necrosis models and drug discovery: a focus on cellular inflammation. Drug Discov Today 11: 364-370, 2006.
18. Jablonski P, Howden BO, Rae DA, Birrel CS, Marshall VC, Tange J. An experimental model for assessment of renal recovery from warm ischemia. Transplantation 35: 198-204, 1983.
19. Jo SK, Bajwa A, Ye H, Vergis AL, Awad AS, Kharel Y, Lynch KR, Okusa MD. Divergent roles of sphingosine kinases in kidney ischemia-reperfusion injury. Kidney Int 75: 167-175, 2009.
20. Jo SK, Rosner MH, Okusa MD. Pharmacologic treatment of acute kidney injury: why drugs haven't worked and what is on the horizon. Clin J Am Soc Nephrol 2: 356-365, 2007.
21. Jones DR, Lee HT. Perioperative renal protection. Best Pract Res Clin Anaesthesiol 22: 193-208, 2008.
22. Kim M, Chen SW, Park SW, Kim M, D'Agati VD, Yang J, Lee HT. Kidney-specific reconstitution of the A1 adenosine receptor in A1 aden-osine receptor knockout mice reduces renal ischemia-reperfusion injury. Kidney Int 75: 809-823, 2009.
23. Kim M, Kim M, Kim N, 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.
24. 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.
25. Kim M, Park SW, Kim M, Chen SW, Gerthoffer WT, D'Agati VD, Lee HT. Selective renal overexpression of human heat shock protein 27 reduces renal ischemia-reperfusion injury in mice. Am J Physiol Renal Physiol 299: F347-F358, 2010.
26. Kimura R, Maeda M, Arita A, Oshima Y, Obana M, Ito T, Yamamoto Y, Mohri T, Kishimoto T, Kawase I, Fujio Y, Azuma J. Identification of cardiac myocytes as the target of interleukin 11, a cardioprotective cytokine. Cytokine 38: 107-115, 2007.
27. Klawitter S, Hofmann LP, Pfeilschifter J, Huwiler A. Extracellular nucleotides induce migration of renal mesangial cells by upregulating sphingosine kinase-1 expression and activity. Br J Pharmacol 150: 271- 280, 2007.
28. Kuenzler KA, Pearson PY, Schwartz MZ. IL-11 pretreatment reduces cell death after intestinal ischemia-reperfusion. J Surg Res 108: 268-272, 2002.
29. Lai PC, Cook HT, Smith J, Keith JC Jr, Pusey CD, Tam FW. Interleukin-11 attenuates nephrotoxic nephritis in Wistar Kyoto rats. J Am Soc Nephrol 12: 2310-2320, 2001.
30. Leclercq TM, Pitson SM. Cellular signalling by sphingosine kinase and sphingosine 1-phosphate. IUBMB Life 58: 467-472, 2006.
31. Lee HT, Emala CW. Adenosine attenuates oxidant injury in human kidney proximal tubular cells via A1 and A2a adenosine receptor activation. Am J Physiol Renal Physiol 282: F844-F852, 2002.
32. Lee HT, Gallos G, Nasr SH, Emala CW. A1 adenosine receptor activation inhibits inflammation, necrosis, and apoptosis after renal ische-mia-reperfusion injury in mice. J Am Soc Nephrol 15: 102-111, 2004.
33. Lee HT, Kim M, Jan M, Penn RB, Emala CW. Renal tubule necrosis and apoptosis modulation by A1 adenosine receptor expression. Kidney Int 71: 1249-1261, 2007.
34. Lee HT, Xu H, Nasr SH, Schnermann J, Emala CW. A1 adenosine receptor knockout mice exhibit increased renal injury following ischemia and reperfusion. Am J Physiol Renal Physiol 286: F298-F306, 2004.
35. Liu H, Chakravarty D, Maceyka M, Milstien S, Spiegel S. Sphingosine kinases: a novel family of lipid kinases. Prog Nucleic Acid Res Mol Biol 71: 493-511, 2002.
36. Mabjeesh NJ, Escuin D, LaVallee TM, Pribluda VS, Swartz GM, Johnson MS, Willard MT, Zhong H, Simons JW, Giannakakou P. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell 3: 363-375, 2003.
37. Mizugishi K, Yamashita T, Olivera A, Miller GF, Spiegel S, Proia RL. Essential role for sphingosine kinases in neural and vascular development. Mol Cell Biol 25: 11113-11121, 2005.
38. Mooberry SL. Mechanism of action of 2-methoxyestradiol: new developments. Drug Resist Updat 6: 355-361, 2003.
39. Naugler KM, Baer KA, Ropeleski MJ. Interleukin-11 antagonizes Fas ligand-mediated apoptosis in IEC-18 intestinal epithelial crypt cells: role of MEK and Akt-dependent signaling. Am J Physiol Gastrointest Liver Physiol 294: G728-G737, 2008.
40. Obana M, Maeda M, Takeda K, Hayama A, Mohri T, Yamashita T, Nakaoka Y, Komuro I, Takeda K, Matsumiya G, Azuma J, Fujio Y. Therapeutic activation of signal transducer and activator of transcription 3 by interleukin-11 ameliorates cardiac fibrosis after myocardial infarction. Circulation 121: 684-691, 2010.
41. Park SW, Kim M, Chen SW, Brown KM, D'Agati VD, Lee HT. Sphinganine-1-phosphate protects kidney and liver after hepatic ischemia and reperfusion in mice through S1P(1) receptor activation. Lab Invest 90: 1209-1224, 2010.
42. Pitman MR, Pham DH, Pitson SM. Isoform-selective assays for sphin-gosine kinase activity. Methods Mol Biol 874: 21-31, 2012.
43. Reynolds CH. Clinical efficacy of rhIL-11. Oncology (Williston Park) 14: 32-40, 2000.
44. Ropeleski MJ, Tang J, Walsh-Reitz MM, Musch MW, Chang EB. Interleukin-11-induced heat shock protein 25 confers intestinal epithelial-specific cytoprotection from oxidant stress. Gastroenterology 124: 1358-1368, 2003.
45. Rosenberger C, Rosen S, Shina A, Frei U, Eckardt KU, Flippin LA, Arend M, Klaus SJ, Heyman SN. Activation of hypoxia-inducible factors ameliorates hypoxic distal tubular injury in the isolated perfused rat kidney. Nephrol Dial Transplant 23: 3472-3478, 2008.
46. Ruff MR, Gifford GE. Rabbit tumor necrosis factor: mechanism of action. Infect Immun 31: 380-385, 1981.
47. Schodel J, Klanke B, Weidemann A, Buchholz B, Bernhardt W, Bertog M, Amann K, Korbmacher C, Wiesener M, Warnecke C, Kurtz A, Eckardt KU, Willam C. HIF-prolyl hydroxylases in the rat kidney: physiologic expression patterns and regulation in acute kidney injury. Am J Pathol 174: 1663-1674, 2009.
48. Schwalm S, Doll F, Romer I, Bubnova S, Pfeilschifter J, Huwiler A. Sphingosine kinase-1 is a hypoxia-regulated gene that stimulates migration of human endothelial cells. Biochem Biophys Res Commun 368: 1020-1025, 2008.
49. Sheridan BC, Dinarello CA, Meldrum DR, Fullerton DA, Selzman CH, McIntyre RC Jr. Interleukin-11 attenuates pulmonary inflammation and vasomotor dysfunction in endotoxin-induced lung injury. Am J Physiol Lung Cell Mol Physiol 277: L861-L867, 1999.
50. Slot C. Plasma creatinine determination. A new and specific Jaffe reaction method. Scand J Clin Lab Invest 17: 381-387, 1965.
51. Smith JW. Tolerability and side-effect profile of rhIL-11. Oncology (Williston Park) 14: 41-47, 2000.
52. Takagi A, Yamashita N, Yoshioka T, Takaishi Y, Sano K, Yamaguchi H, Maeda A, Saito K, Takakura Y, Hashida M. Enhanced pharmacological activity of recombinant human interleukin-11 (rhIL11) by chemical modification with polyethylene glycol. J Control Release 119: 271-278, 2007.
53. Trepicchio WL, Bozza M, Pedneault G, Dorner AJ. Recombinant human IL-11 attenuates the inflammatory response through down-regulation of proinflammatory cytokine release and nitric oxide production. J Immunol 157: 3627-3634, 1996.
54. Trepicchio WL, Dorner AJ. The therapeutic utility of Interleukin-11 in the treatment of inflammatory disease. Expert Opin Investig Drugs 7: 1501-1504, 1998.
55. Trepicchio WL, Wang L, Bozza M, Dorner AJ. IL-11 regulates mac-rophage effector function through the inhibition of nuclear factor-kappaB. J Immunol 159: 5661-5670, 1997.
56. Venkataraman K, Thangada S, Michaud J, Oo ML, Ai Y, Lee YM, Wu M, Parikh NS, Khan F, Proia RL, Hla T. Extracellular export of sphingosine kinase-1a contributes to the vascular S1P gradient. Biochem J 397: 461-471, 2006.
57. Vessey DA, Kelley M, Karliner JS. A rapid radioassay for sphingosine kinase. Anal Biochem 337: 136-142, 2005.
58. Vessey DA, Kelley M, Li L, Huang Y, Zhou HZ, Zhu BQ, Karliner JS. Role of sphingosine kinase activity in protection of heart against ischemia reperfusion injury. Med Sci Monit 12: BR318-BR324, 2006.
59. Volpi G, Facchinetti F, Moretto N, Civelli M, Patacchini R. Cigarette smoke and alpha,beta-unsaturated aldehydes elicit VEGF release through the p38 MAPK pathway in human airway smooth muscle cells and lung fibroblasts. Br J Pharmacol 163: 649-661, 2011.
60. Wadgaonkar R, Patel V, Grinkina N, Romano C, Liu J, Zhao Y, Sammani S, Garcia JG, Natarajan V. Differential regulation of sphin-gosine kinases 1 and 2 in lung injury. Am J Physiol Lung Cell Mol Physiol 296: L603-L613, 2009.
61. Waxman AB, Mahboubi K, Knickelbein RG, Mantell LL, Manzo N, Pober JS, Elias JA. Interleukin-11 and interleukin-6 protect cultured human endothelial cells from H2O2-induced cell death. Am J Respir Cell Mol Biol 29: 513-522, 2003.
62. Wright SC, Kumar P, Tam AW, Shen N, Varma M, Larrick JW. Apoptosis and DNA fragmentation precede TNF-induced cytolysis in U937 cells. J Cell Biochem 48: 344-355, 1992.
63. Wu Y, Dong Y, Song P, Zou MH. Activation of the AMP-activated protein kinase (AMPK) by nitrated lipids in endothelial cells. PLoS One 7: e31056, 2012.
64. Yeo EJ, Chun YS, Cho YS, Kim J, Lee JC, Kim MS, Park JW. YC-1: a potential anticancer drug targeting hypoxia-inducible factor 1. J Natl Cancer Inst 95: 516-525, 2003.