Development of oxidative stress in the peritubular capillary microenvironment mediates sepsis-induced renal microcirculatory failure and acute kidney injury

American Journal of Pathology

Volumn 180, Issue 2, 2012, Pages 505-516

  Wang, Zhen ^a   Holthoff, Joseph H ^a   Seely, Kathryn A ^a   Pathak, Elina ^a   Spencer III, Horace J ^a   Gokden, Neriman ^a   Mayeux, Philip R ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

[MANGANESE TETRAKIS( 1 METHYL 4 PYRIDYL)PORPHYRIN, TETRATOSYLATE, HYDROXIDE]; CILASTATIN PLUS IMIPENEM; PEROXYNITRITE; PORPHYRIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY PERMEABILITY; CONTROLLED STUDY; DRUG MECHANISM; GLOMERULUS FILTRATION RATE; HYPOXIA; KIDNEY BLOOD FLOW; KIDNEY BLOOD VESSEL; KIDNEY CIRCULATION; KIDNEY FUNCTION; KIDNEY PERFUSION; KIDNEY TUBULE; MALE; MEAN ARTERIAL PRESSURE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SEPSIS; SURVIVAL TIME;

ACUTE KIDNEY INJURY; ANIMALS; BLOOD PRESSURE; CAPILLARIES; CAPILLARY PERMEABILITY; CELL HYPOXIA; CELLULAR MICROENVIRONMENT; EPITHELIAL CELLS; FREE RADICAL SCAVENGERS; GLOMERULAR FILTRATION RATE; HEART RATE; LIGATION; MALE; METALLOPORPHYRINS; MICE; MICE, INBRED C57BL; NITRATES; NITRITES; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; RENAL CIRCULATION; SEPSIS; SUPEROXIDE DISMUTASE;

EID: 84856018760     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.10.011     Document Type: Article

References (65)

1. S. Heemskerk, R. Masereeuw, F.G. Russel, P. Pickkers Selective iNOS inhibition for the treatment of sepsis-induced AKI Nat Rev Nephrol 5 2009 629 640
2. S.M. Bagshaw, S. Lapinsky, S. Dial, Y. Arabi, P. Dodek, G. Wood, P. Ellis, J. Guzman, J. Marshall, J.E. Parrillo, Y. Skrobik, A. Kumar Acute kidney injury in septic shock: clinical outcomes and impact of duration of hypotension prior to initiation of antimicrobial therapy Intensive Care Med 35 2009 871 881
3. Z. Ricci, A. Polito, C. Ronco The implications and management of septic acute kidney injury Nat Rev Nephrol 7 2011 218 225
4. M.M. Levy, R.P. Dellinger, S.R. Townsend, W.T. Linde-Zwirble, J.C. Marshall, J. Bion, C. Schorr, A. Artigas, G. Ramsay, R. Beale, M.M. Parker, H. Gerlach, K. Reinhart, E. Silva, M. Harvey, S. Regan, D.C. Angus The Surviving Sepsis Campaign: results of an international guideline-based performance improvement program targeting severe sepsis Crit Care Med 38 2010 367 374
5. Y. Sakr, M.J. Dubois, D. De Backer, J. Creteur, J.L. Vincent Persistent microcirculatory alterations are associated with organ failure and death in patients with septic shock Crit Care Med 32 2004 1825 1831
6. J.L. Vincent, D. De Backer Microvascular dysfunction as a cause of organ dysfunction in severe sepsis Crit Care 9 Suppl 4 2005 S9 S12
7. C. Dudley Maximizing renal preservation in acute renal failure BJU Int 94 2004 1202 1206
8. T. Miyaji, X. Hu, P.S. Yuen, Y. Muramatsu, S. Iyer, S.M. Hewitt, R.A. Star Ethyl pyruvate decreases sepsis-induced acute renal failure and multiple organ damage in aged mice Kidney Int 64 2003 1620 1631
9. E.D. Crouser Mitochondrial dysfunction in septic shock and multiple organ dysfunction syndrome Mitochondrion 4 2004 729 741
10. H.F. Galley Bench-to-bedside review: targeting antioxidants to mitochondria in sepsis Crit Care 14 2010 230
11. D. Brealey, M. Brand, I. Hargreaves, S. Heales, J. Land, R. Smolenski, N.A. Davies, C.E. Cooper, M. Singer Association between mitochondrial dysfunction and severity and outcome of septic shock Lancet 360 2002 219 223
12. H.F. Goode, H.C. Cowley, B.E. Walker, P.D. Howdle, N.R. Webster Decreased antioxidant status and increased lipid peroxidation in patients with septic shock and secondary organ dysfunction Crit Care Med 23 1995 646 651
13. A. Spanos, S. Jhanji, A. Vivian-Smith, T. Harris, R.M. Pearse Early microvascular changes in sepsis and severe sepsis Shock 33 2010 387 391
14. L. Wu, N. Gokden, P.R. Mayeux Evidence for the role of reactive nitrogen species in polymicrobial sepsis-induced renal peritubular capillary dysfunction and tubular injury J Am Soc Nephrol 18 2007 1807 1815
15. L. Wu, P.R. Mayeux Effects of the inducible nitric oxide synthase inhibitor L-N6-(1-iminoethyl)-lysine on microcirculation and reactive nitrogen species generation in the kidney following lipopolysaccharide administration in mice J Pharmacol Exp Ther 320 2007 1061 1067
16. W. Wang, S. Jittikanont, S.A. Falk, P. Li, L. Feng, P.E. Gengaro, B.D. Poole, R.P. Bowler, B.J. Day, J.D. Crapo, R.W. Schrier Interaction among nitric oxide, reactive oxygen species, and antioxidants during endotoxemia-related acute renal failure Am J Physiol Renal Physiol 284 2003 F532 F537
17. K.M. Faulkner, S.I. Liochev, I. Fridovich Stable Mn(III) porphyrins mimic superoxide dismutase in vitro and substitute for it in vivo J Biol Chem 269 1994 23471 23476
18. J.P. Crow Peroxynitrite scavenging by metalloporphyrins and thiolates Free Rad Biol Med 28 2000 1487 1494
19. Z. Qi, I. Whitt, A. Mehta, J. Jin, M. Zhao, R.C. Harris, A.B. Fogo, M.D. Breyer Serial determination of glomerular filtration rate in conscious mice using FITC-inulin clearance Am J Physiol Renal Physiol 286 2004 F590 F596
20. Z. Wang, C. Herzog, G.P. Kaushal, N. Gokden, P.R. Mayeux Actinonin, a meprin A inhibitor, protects the renal microcirculation during sepsis Shock 35 2011 141 147
21. L. Wu, M.M. Tiwari, K.J. Messer, J.H. Holthoff, N. Gokden, R.W. Brock, P.R. Mayeux Peritubular capillary dysfunction and renal tubular epithelial cell stress following lipopolysaccharide administration in mice Am J Physiol Renal Physiol 292 2007 F261 F268
22. A. Gomes, E. Fernandes, J.L. Lima Use of fluorescence probes for detection of reactive nitrogen species: a review J Fluoresc 16 2006 119 139
23. K.M. Robinson, M.S. Janes, M. Pehar, J.S. Monette, M.F. Ross, T.M. Hagen, M.P. Murphy, J.S. Beckman Selective fluorescent imaging of superoxide in vivo using ethidium-based probes Proc Natl Acad Sci USA 103 2006 15038 15043
24. M. Paxian, S.A. Keller, B. Cross, T.T. Huynh, M.G. Clemens High-resolution visualization of oxygen distribution in the liver in vivo Am J Physiol Gastrointest Liver Physiol 286 2004 G37 G44
25. C. Wunder, R.W. Brock, A. Krug, N. Roewer, O. Eichelbronner A remission spectroscopy system for in vivo monitoring of hemoglobin oxygen saturation in murine hepatic sinusoids, in early systemic inflammation Comp Hepatol 4 2005 1 10.1186/1476-5926-4-1
26. H. Yasuda, P.S. Yuen, X. Hu, H. Zhou, R.A. Star Simvastatin improves sepsis-induced mortality and acute kidney injury via renal vascular effects Kidney Int 69 2006 1535 1542
27. J. Moitra, S. Sammani, J.G. Garcia Re-evaluation of Evans Blue dye as a marker of albumin clearance in murine models of acute lung injury Trans Res 150 2007 253 265
28. G.E. Arteel, R.G. Thurman, J.A. Raleigh Reductive metabolism of the hypoxia marker pimonidazole is regulated by oxygen tension independent of the pyridine nucleotide redox state Eur J Biochem 253 1998 743 750
29. W. Wang, S. Faubel, D. Ljubanovic, A. Mitra, J. Kim, Y. Tao, A. Soloviev, L.L. Reznikov, C.A. Dinarello, R.W. Schrier, C.L. Edelstein Endotoxemic acute renal failure (ARF) is attenuated in caspase-1 deficient mice Am J Physiol Renal Physiol 288 2005 F997 F1004
30. J. Mortensen, B. Shames, C.P. Johnson, V. Nilakantan MnTMPyP, a superoxide dismutase/catalase mimetic, decreases inflammatory indices in ischemic acute kidney injury Inflamm Res 60 2011 299 307
31. N. Nin, A. Cassina, J. Boggia, E. Alfonso, H. Botti, G. Peluffo, A. Trostchansky, C. Batthyany, R. Radi, H. Rubbo, F.J. Hurtado Septic diaphragmatic dysfunction is prevented by Mn(III)porphyrin therapy and inducible nitric oxide synthase inhibition Intensive Care Med 30 2004 2271 2278
32. P.A. Warn, M.W. Brampton, A. Sharp, G. Morrissey, N. Steel, D.W. Denning, T. Priest Infrared body temperature measurement of mice as an early predictor of death in experimental fungal infections Lab Anim 37 2003 126 131
33. V. Vallon, T. Traynor, L. Barajas, Y.G. Huang, J.P. Briggs, J. Schnermann Feedback control of glomerular vascular tone in neuronal nitric oxide synthase knockout mice J Am Soc Nephrol 12 2001 1599 1606
34. S. Heemskerk, P. Pickkers, M.P. Bouw, A. Draisma, J.G. van der Hoeven, W.H. Peters, P. Smits, F.G. Russel, R. Masereeuw Upregulation of renal inducible nitric oxide synthase during human endotoxemia and sepsis is associated with proximal tubule injury Clin J Am Soc Nephrol 1 2006 853 862
35. P. Kumar, Q. Shen, C.D. Pivetti, E.S. Lee, M.H. Wu, S.Y. Yuan Molecular mechanisms of endothelial hyperpermeability: implications in inflammation Expert Rev Mol Med 11 2009 e19
36. J.S. Beckman Oxidative damage and tyrosine nitration from peroxynitrite Chem Res Tox 9 1996 836 844
37. K. Doi, P.S. Yuen, C. Eisner, X. Hu, A. Leelahavanichkul, J. Schnermann, R.A. Star Reduced production of creatinine limits its use as marker of kidney injury in sepsis J Am Soc Nephrol 20 2009 1217 1221
38. I. Batinic-Haberle, J.S. Reboucas, I. Spasojevic Superoxide dismutase mimics: chemistry, pharmacology, and therapeutic potential Antioxid Redox Signal 13 2010 877 918
39. K. Doi, A. Leelahavanichkul, P.S. Yuen, R.A. Star Animal models of sepsis and sepsis-induced kidney injury J Clin Invest 119 2009 2868 2878
40. S. Villalpando, J. Gopal, A. Balasubramanyam, V.P. Bandi, K. Guntupalli, F. Jahoor In vivo arginine production and intravascular nitric oxide synthesis in hypotensive sepsis Am J Clin Nutr 84 2006 197 203
41. R. Murugan, J.A. Kellum Acute kidney injury: what's the prognosis? Nat Rev Nephrol 7 2011 209 217
42. L. Wan, S.M. Bagshaw, C. Langenberg, T. Saotome, C. May, R. Bellomo Pathophysiology of septic acute kidney injury: what do we really know? Crit Care Med 36 2008 S198 S203
43. C. Langenberg, L. Wan, M. Egi, C.N. May, R. Bellomo Renal blood flow in experimental septic acute renal failure Kidney Int 69 2006 1996 2002
44. R. Ramchandra, L. Wan, S.G. Hood, R. Frithiof, R. Bellomo, C.N. May Septic shock induces distinct changes in sympathetic nerve activity to the heart and kidney in conscious sheep Am J Physiol Regul Integr Comp Physiol 297 2009 R1247 R1253
45. S. Brandt, T. Regueira, H. Bracht, F. Porta, S. Djafarzadeh, J. Takala, J. Gorrasi, E. Borotto, V. Krejci, L.B. Hiltebrand, L.E. Bruegger, G. Beldi, L. Wilkens, P.M. Lepper, U. Kessler, S.M. Jakob Effect of fluid resuscitation on mortality and organ function in experimental sepsis models Crit Care 13 2009 R186
46. J. Chvojka, R. Sykora, A. Krouzecky, J. Radej, V. Varnerova, T. Karvunidis, O. Hes, I. Novak, P. Radermacher, M. Matejovic Renal haemodynamic, microcirculatory, metabolic and histopathological responses to peritonitis-induced septic shock in pigs Crit Care 12 2008 R164
47. V.E. Bradley, M.R. Shier, C.E. Lucas, I.K. Rosenberg Renal hemodynamic response to furosemide in septic and injured patients Surgery 79 1976 549 554
48. M. Brenner, G.L. Schaer, D.L. Mallory, A.F. Suffredini, J.E. Parrillo Detection of renal blood flow abnormalities in septic and critically ill patients using a newly designed indwelling thermodilution renal vein catheter Chest 98 1990 170 179
49. W.L. Lee, A.S. Slutsky Sepsis and endothelial permeability N Engl J Med 363 2010 689 691
50. J.J. Boffa, A. Just, T.M. Coffman, W.J. Arendshorst Thromboxane receptor mediates renal vasoconstriction and contributes to acute renal failure in endotoxemic mice J Am Soc Nephrol 15 2004 2358 2365
51. T.A. Sutton Alteration of microvascular permeability in acute kidney injury Microvasc Res 77 2009 4 7
52. D.J. Stearns-Kurosawa, M.F. Osuchowski, C. Valentine, S. Kurosawa, D.G. Remick The pathogenesis of sepsis Annu Rev Pathol 6 2011 19 48
53. T. Okamoto, T. Akaike, T. Sawa, Y. Miyamoto, A. van der Vliet, H. Maeda Activation of matrix metalloproteinases by peroxynitrite-induced protein Sglutathiolation via disulfide Soxide formation J Biol Chem 276 2001 29596 29602
54. R. Radi, M. Rodriguez, L. Castro, R. Telleri Inhibition of mitochondrial electron transport by peroxynitrite Arch Biochem Biophys 308 1994 89 95
55. A. Just, C.L. Whitten, W.J. Arendshorst Reactive oxygen species participate in acute renal vasoconstrictor responses induced by ETA and ETB receptors Am J Physiol Renal Physiol 294 2008 F719 F728
56. D.S. Majid, A. Nishiyama, K.E. Jackson, A. Castillo Superoxide scavenging attenuates renal responses to ANG II during nitric oxide synthase inhibition in anesthetized dogs Am J Physiol Renal Physiol 288 2005 F412 F419
57. L.C. Matavelli, P.J. Kadowitz, L.G. Navar, D.S. Majid Renal hemodynamic and excretory responses to intra-arterial infusion of peroxynitrite in anesthetized rats Am J Physiol Renal Physiol 296 2009 F170 F176
58. N. Nin, M. El-Assar, C. Sanchez, A. Ferruelo, A. Sanchez-Ferrer, L. Martinez-Caro, Y. Rojas, M. de Paula, J. Hurtado, A. Esteban, J.A. Lorente Vascular dysfunction in sepsis: effects of the peroxynitrite decomposition catalyst MnTMPyP Shock 36 2011 156 161
59. M.M. Tiwari, R.W. Brock, G.P. Kaushal, P.R. Mayeux Disruption of renal peritubular blood flow in lipopolysaccharide-induced renal failure: role of nitric oxide and caspases Am J Physiol Renal Physiol 289 2005 F1324 F1332
60. M.D. Okusa The changing pattern of acute kidney injury: from one to multiple organ failure Contrib Nephrol 165 2010 153 158
61. E. Crimi, V. Sica, S. Williams-Ignarro, H. Zhang, A.S. Slutsky, L.J. Ignarro, C. Napoli The role of oxidative stress in adult critical care Free Rad Biol Med 40 2006 398 406
62. V. Nilakantan, H.L. Liang, S. Rajesh, J. Mortensen, K. Chandran Time-dependent protective effects of manganese(III) tetrakis (1-methyl-4-pyridyl) porphyrin on mitochondrial function following renal ischemia-reperfusion injury Free Radic Res 44 2010 773 782
63. K. Doi, X. Hu, P.S. Yuen, A. Leelahavanichkul, H. Yasuda, S.M. Kim, J. Schnermann, T.E. Jonassen, J. Frokiaer, S. Nielsen, R.A. Star AP214, an analogue of alpha-melanocytestimulating hormone, ameliorates sepsis-induced acute kidney injury and mortality Kidney Int 73 2008 1266 1274
64. A. Leelahavanichkul, H. Yasuda, K. Doi, X. Hu, H. Zhou, P.S. Yuen, R.A. Star Methyl-2-acetamidoacrylate, an ethyl pyruvate analog, decreases sepsis-induced acute kidney injury in mice Am J Physiol Renal Physiol 295 2008 F1825 F1835
65. J.H. Holthoff, Z. Wang, K.A. Seely, N. Gokden, P.R. Mayeux Resveratrol improves renal microcirculation, protects the tubular epithelium, and prolongs survival in a mouse model of sepsis-induced acute kidney injury Kidney Int 2011 10.1038/ki.2011.347