5-Lypoxygenase products are involved in renal tubulointerstitial injury induced by albumin overload in proximal tubules in mice

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Landgraf, Sharon Schilling ^a,b   Silva, Leandro Souza ^a   Peruchetti, Diogo Barros ^a   Sirtoli, Gabriela Modenesi ^a   Moraes Santos, Felipe ^a   Portella, Viviane Gomes ^a   Silva Filho, João Luiz ^a   Pinheiro, Carla Silva ^a   Abreu, Thiago Pereira ^a   Takiya, Christina Maeda ^a   Benjamin, Claudia Farias ^a   Pinheiro, Ana Acacia Sá ^a   Canetti, Claudio ^a   Caruso Neves, Celso ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO FEDERAL DE EDUCAÇÃO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

5 LYPOXYGENASE; ALBUMIN; INTERLEUKIN 10; INTERLEUKIN 6; LACTATE DEHYDROGENASE; LEUKOTRIENE B4; LEUKOTRIENE D4; NESTIN; OXYGENASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE C; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ARACHIDONATE 5 LIPOXYGENASE; SERUM ALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE DAMAGE; MACROPHAGE MIGRATION; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN URINE LEVEL; SIGNAL TRANSDUCTION; TUBULOINTERSTITIAL INJURY; WILD TYPE; ANIMAL; BOVINE; CELL LINE; COMPLICATION; DISEASE MODEL; GENE DELETION; GENETICS; GLOMERULUS; KIDNEY DISEASES; METABOLISM; PATHOLOGY; PIG; PROTEINURIA;

MUS;

ANIMALS; ARACHIDONATE 5-LIPOXYGENASE; CATTLE; CELL LINE; DISEASE MODELS, ANIMAL; GENE DELETION; KIDNEY DISEASES; KIDNEY GLOMERULUS; KIDNEY TUBULES, PROXIMAL; MALE; MICE; PROTEINURIA; SERUM ALBUMIN; SWINE;

EID: 84907828114     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107549     Document Type: Article

References (81)

1. Rinaldo-Matthis A, Haeggstrom JZ (2010) Structures and mechanisms of enzymes in the leukotriene cascade. Biochimie 92: 676-681.
2. Hao CM, Breyer MD (2007) Physiologic and pathophysiologic roles of lipid mediators in the kidney. Kidney Int 71: 1105-1115.
3. Woods JW, Evans JF, Ethier D, Scott S, Vickers PJ, et al. (1993) 5-Lipoxygenase and 5-lipoxygenase-activating protein are localized in the nuclear envelope of activated human leukocytes. J Exp Med 178: 1935-1946.
4. Hedi H, Norbert G (2004) 5-Lipoxygenase pathway, dendritic cells, and adaptive immunity. J Biomed Biotechnol 2: 99-105.
5. Luchtefeld M, Drexler H, Schieffer B (2003) 5-Lipoxygenase is involved in the angiotensin II-induced NAD(P)H-oxidase activation. Biochem Biophys Res Commun 308: 668-672.
6. Reinhold SW, Vitzthum H, Filbeck T, Wolf K, Lattas C, et al. (2006) Gene expression of 5-, 12-, and 15-lipoxygenases and leukotriene receptors along the rat nephron. Am J Physiol Renal Physiol 290: F864-F872.
7. Moore KP, Wood J, Gove C, Tan KC, Eason J, et al. (1991) Synthesis and metabolism of cysteinyl leukotrienes by the isolated pig kidney. Adv Prostaglandin Thromboxane Leukot Res 21B: 697-700.
8. Sener G, Sakarcan A, Sehirli O, Eksioʇlu-Demiralp E, Sener E, et al. (2007) Chronic renal failure-induced multiple-organ injury in rats is alleviated by the selective CysLT1 receptor antagonist montelukast. Prostaglandins Other Lipid Mediat 83: 257-267.
9. Peters-Golden M, Henderson WR Jr (2007) Leukotrienes. N Engl J Med 357: 1841-1854.
10. 5production from stimulated neutrophil granulocytes in patients with chronic kidney disease. Prostaglandins Leukot Essent Fatty Acids. 85(1): 37-41.
11. Taccone-Gallucci M, Maccarrone M, Manca di Villahermosa S, Meloni C, Finazzi Agrò A (2000) Lipoperoxidation in hemodialysis patients: upregulation of 5-lipoxygenase activity and expression in peripheral blood mononuclear cells. Contrib Nephrol 130: 130-133.
12. Taccone-Gallucci M, Manca-di-Villahermosa S, Battistini L, Stuffler RG, Tedesco M, et al. (2006) N-3 PUFAs reduce oxidative stress in ESRD patients on maintenance HD by inhibiting 5-lipoxygenase activity. Kidney Int 69: 1450-1454.
13. Petric R, Ford-Hutchinson A (1995) Inhibition of leukotriene biosynthesis improves renal function in experimental glomerulonephritis. J Lipid Mediat Cell Signal 11: 231-240.
14. Atakan A, Arikan H, Macunluoglu B, Tuglular S, Ulfer G, et al. (2008) Renal protective effects of leukotriene receptor blockers in an experimental model of cyclosporine nephrotoxicity. Transplant Proc 40: 279-284.
15. Hadi NR, Al-amran FG, Hussein AA (2011) Effects of thyroid hormone analogue and a leukotrienes pathway-blocker on renal ischemia/reperfusion injury in mice. BMC Nephrol 12: 70.
16. Hagar HH, Abd El Tawab R (2012) Cysteinyl leukotriene receptor antagonism alleviates renal injury induced by ischemia-reperfusion in rats. J Surg Res 178: e25-34.
17. Matsuyama M, Funao K, Chargui J, Touraine JL, Nakatani T, et al. (2009) The role of cysteinyl-LT(1)receptor (CysLT(1)R) in renal ischemia-reperfusion injury. Transplant Proc 41: 73-75.
18. Patel NS, Cuzzocrea S, Chatterjee PK, Di Paola R, Sautebin L, et al. (2004) Reduction of renal ischemia-reperfusion injury in 5-lipoxygenase knockout mice and by the 5-lipoxygenase inhibitor zileuton. Mol Pharmacol 66: 220-227.
19. Sener G, Sehirli O, Velioʇlu-Oʇünc¸ A, Cetinel S, Gedik N, et al. (2006) Montelukast protects against renal ischemia/reperfusion injury in rats. Pharmacol Res 54: 65-71.
20. Gorriz JL, Martinez-Castelao A (2012) Proteinuria: detection and role in native renal disease progression. Transplant Rev (Orlando) 26: 3-13.
21. Poudel B, Yadav BK, Nepal AK, Jha B, Raut KB (2012) Prevalence and association of microalbuminuria in essential hypertensive patients. N Am J Med Sci 4: 331-335.
22. Abbate M, Zoja C, Remuzzi G (2006) How does proteinuria cause progressive renal damage? J Am Soc Nephrol 7: 2974-2984.
23. Caruso-Neves C, Pinheiro AAS, Cai H, Souza-Menezes J, Guggino WB (2006) PKB and megalin determine the survival or death of renal proximal tubule cells. Proc Natl Acad Sci U S A 103: 18810-18815.
24. Thomas ME, Brunskill NJ, Harris KP, Bailey E, Pringle JH, et al. (1999) Proteinuria induces tubular cell turnover: a potential mechanism for tubular atrophy. Kidney Int 55(3): 890-898.
25. Ishola DA Jr, van der Giezen DM, Hahnel B, Goldschmeding R, Kriz W, et al. (2006) In mice, proteinuria and renal inflammatory responses to albumin overload are strain-dependent. Nephrol Dial Transplant 21: 591-597.
26. Portella VG, Silva-Filho JL, Landgraf SS, de Rico TB, Vieira MA, et al. (2013) Sepsis-surviving mice are more susceptible to a secondary kidney insult. Crit Care Med 41: 1056-1068.
27. Eddy AA (1989) Interstitial nephritis induced by protein-overload proteinuria. Am J Pathol 135: 719-733.
28. Ishola DA Jr, van der Giezen DM, Hahnel B, Goldschmeding R, Kriz W, et al. (2006) In mice, proteinuria and renal inflammatory responses to albumin overload are strain-dependent. Nephrol Dial Transplant 21: 591-7.
29. Abreu TP, Silva LS, Takiya CM, Souza MC, Henriques MG, et al. (2014) Mice rescued from severe malaria are protected against renal injury during a second kidney insult. PLoS One 9:e93634.
30. Landgraf SS, Wengert M, Silva JS, Zapata-Sudo G, Sudo RT, et al. (2011) Changes in angiotensin receptors expression play a pivotal role in the renal damage observed in spontaneously hypertensive rats. Am J Physiol Renal Physiol 300: F499-F510.
31. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
32. Gekle M, Knaus P, Nielsen R, Mildenberger S, Freudinger R, et al. (2003) Transforming growth factor-beta1 reduces megalin- and cubilin-mediated endocytosis of albumin in proximal-tubule-derived opossum kidney cells. J Physiol 552: 471-481.
33. Caruso-Neves C, Kwon SH, Guggino WB (2005) Albumin endocytosis in proximal tubule cells is modulated by angiotensin II through an AT2 receptor-mediated protein kinase B activation. Proc Natl Acad Sci U S A 102: 17513-17518.
34. +)-ATPase is a target for phosphoinositide 3-kinase/protein kinase B and protein kinase C pathways triggered by albumin. J Biol Chem 286: 45041-45047.
35. Su W, Chen J, Yang H, You L, Xu L, et al. (2007) Expression of nestin in the podocytes of normal and diseased human kidneys. Am J Physiol Regul Integr Comp Physiol 292: R1761-R1767.
36. Gekle M, Mildenberger S, Freudinger R, Schwerdt G, Silbernagl S (1997) Albumin endocytosis in OK cells: dependence on actin and microtubules and regulation by protein kinases. Am J Physiol 272(5 Pt 2): F668-F677.
37. Câmara NO, Martins JO, Landgraf RG, Jancar S (2009) Emerging roles for eicosanoids in renal diseases. Curr Opin Nephrol Hypertens 18: 21-27.
38. Valdivielso JM, Montero A, Badr KF, Munger KA (2003) Inhibition of 5-lipoxygenase activating protein decreases proteinuria in diabetic rats. J Nephrol 16: 85-94.
39. Guasch A, Zayas CF, Badr KF (1999) MK-591 acutely restores glomerular size selectivity and reduces proteinuria in human glomerulonephritis. Kidney Int 56: 261-267.
40. Hefler LA, Tempfer CB, Moreno RM, O'Brien WE, Gregg AR (2001) Endothelial derived nitric oxide and angiotensinogen: blood pressure and metabolism during mouse pregnancy. Am J Physiol Regul Integr Comp Physiol 280: R174-R182.
41. Babelova A, Avaniadi D, Jung O, Fork C, Beckmann J, et al. (2012) Role of Nox4 in murine models of kidney disease. Free Radic Biol Med 53: 842-853.
42. Goulet JL, Griffiths RC, Ruiz P, Mannon RB, Flannery P, et al. (2001) Deficiency of 5-lipoxygenase accelerates renal allograft rejection in mice. J Immunol 167: 6631-6636.
43. Schock-Kusch D, Geraci S, Ermeling E, Shulhevich Y, Sticht C, et al. (2013) Reliability of transcutaneous measurement of renal function in various strains of conscious mice. PLoS One 8: e71519.
44. Katoh T, Lianos EA, Fukunaga M, Takahashi K, Badr KF (1993) Leukotriene D4 is a mediator of proteinuria and glomerular hemodynamic abnormalities in passive Heymann nephritis. J Clin Invest 91: 1507-1515.
45. Brunskill NJ, Stuart J, Tobin AB, Walls J, Nahorski S (1998) Receptor-mediated endocytosis of albumin by kidney proximal tubule cells is regulated by phosphatidylinositide 3-kinase. J Clin Invest 101: 2140-2150.
46. Gekle M, Mildenberger S, Freudinger R, Silbernagl S (1998) Long-term protein exposure reduces albumin binding and uptake in proximal tubule-derived opossum kidney cells. J Am Soc Nephrol 9: 960-968.
47. Ahn KS, Aggarwal BB (2005) Transcription factor NF-κB: A sensor for smoke and stress signals. Ann NY Acad Sci 1056: 218-233.
48. Yu BP, Chung HY (2006) Adaptive mechanisms to oxidative stress during aging. Mech Ageing Dev 127: 436-443.
49. Chung HY, Kim HJ, Kim KW, Choi JS, Yu BP (2002) Molecular inflammation hypothesis of aging based on the anti-aging mechanism of calorie restriction. Microsc Res Tech 59: 264-272.
50. Christman JW, Blackwell TS, Juurlink BH (2000) Redox regulation of nuclear factor kappa B: therapeutic potential for attenuating inflammatory responses. Brain Pathol 10: 153-162.
51. Won JS, Im YB, Khan M, Singh AK, Singh I (2005) Involvement of phospholipase A(2) and lipoxygenase in lipopolysaccharide induced inducible nitric oxide synthase expression in glial cells. Glia 51: 13-21.
52. Bonizzi G, Piette J, Schoonbroodt S, Greimers R, Havard L, et al. (1999) Reactive oxygen intermediate dependent NF-kappaB activation by interleukin-1beta requires 5-lipoxygenase or NADPH oxidase activity. Mol Cell Biol 19: 1950-1960.
53. Jatana M, Giri S, Ansari MA, Elango C, Singh AK, et al. (2006) Inhibition of NF-kB activation by 5-lipoxygenase inhibitors protects brain against injury in a rat model of focal cerebral ischemia. J Neuroinflamm 11: 12.
54. Aoki Y, Qiu D, Zhao GH, Kao PN (1998) Leukotriene B4 mediates histamine induction of NF-kappaB and IL-8 in human bronchial epithelial cells. Am J Physiol 274: 1030-1039.
55. Brach MA, de Vos S, Arnold C, Gruss HJ, Mertelsmann R, et al. (1992) Leukotriene B4 transcriptionally activates interleukin-6 expression involving NK-chi B and NF-IL6. Eur J Immunol 22: 2705-2711.
56. Brock TG (2005) Regulating leukotriene synthesis: The role of nuclear 5-lipoxygenase. J Cell Biochem 96: 1203-1211.
57. Lepley RA, Fitzpatrick FA (1998) 5-Lipoxygenase compartmentalization in granulocytic cells is modulated by an internal bipartite nuclear localizing sequence and nuclear factor kappa B complex formation. Arch Biochem Biophys 356: 71-76.
58. McDonald PP, Bald A, Cassatella MA (1997) Activation of the NF-kappaB pathway by inflammatory stimuli in human neutrophils. Blood 89: 3421-3433.
59. Morigi M, Macconi D, Zoja C, Donadelli R, Buelli S, et al. (2002) Protein overload-induced NF-kappaB activation in proximal tubular cells requires H(2)O(2) through a PKC-dependent pathway. J Am Soc Nephrol 13: 1179-89.
60. Monteiro AP, Pinheiro CS, Luna-Gomes T, Alves LR, Maya-Monteiro CM, et al. (2011) Leukotriene B4 mediates neutrophil migration induced by heme. J Immunol 186: 6562-6567.
61. Heemann U, Szabo A, Hamar P, Muller V, Witzke O, et al. (2000) Lipopolysaccharide pretreatment protects from renal ischemia/reperfusion injury: possible connection to an interleukin-6-dependent pathway. Am J Pathol 156: 287-293.
62. Takada M, Nadeau KC, Shaw GD, Marquette KA, Tilney NL (1997) The cytokine-adhesion molecule cascade in ischemia/reperfusion injury of the rat kidney: inhibition by a soluble P-selectin ligand. J Clin Investig 99: 2682-2690.
63. Patel NS, Chatterjee PK, Di Paola R, Mazzon E, Britti D, et al. (2005) Endogenous interleukin 6 enhances the renal injury, dysfunction, and inflammation caused by ischemia/reperfusion. J Pharmacol Exp Ther 312: 1170-8.
64. Nechemia-Arbely Y, Barkan D, Pizov G, Shriki A, Rose-John S, et al. (2008) IL-6/IL-6R axis plays a critical role in acute kidney injury. J Am Soc Nephrol 19: 1106-15.
65. Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S (2011) The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta 1813: 878-88.
66. Trautwein T, Rakemann M, Niehof S, Rose-John MP (1996) Manns, Acute-phase response factor, increased binding, and target gene transcription during liver regeneration. Gastroenterol 110: 1854-1862.
67. Cressman DE, Greenbaum LE, DeAngelis RA, Ciliberto G, Furth EE, et al. (1996) Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science 274: 1379-1383.
68. Yokota N, O'Donnell M, Daniels F, Burne-Taney M, Keane W, et al. (2003) Protective effect of HMG-CoA reductase inhibitor on experimental renal ischemia-reperfusion injury. Am J Nephrol 23: 13-17.
69. Sun Z, Klein AS, Radaeva S, Hong F, El Assal O, et al. (2003) In vitro interleukin-6 treatment prevents mortality associated with fatty liver transplants in rats. Gastroenterology 125: 202-215.
70. Herrmann O, Tarabin V, Suzuki S, Attigah N, Coserea I, et al. (2003) Regulation of body temperature and neuroprotection by endogenous interleukin-6 in cerebral ischemia. J Cereb Blood Flow Metab 23: 406-415.
71. Xing Z, Gauldie J, Cox G, Baumann H, Jordana M, et al. (1998) IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Invest 101: 311-32.
72. Chalaris A, Rabe B, Paliga K, Lange H, Laskay T, et al. (2007) Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils. Blood 110: 1748-1755.
73. Lakkis FG, Baddoura FK, Cruet EN, Parekh KR, Fukunaga M, et al. (1996) Anti-inflammatory lymphokine mRNA expression in antibody-induced glomerulonephritis. Kidney Int 49: 117-126.
74. Mys̈liwska J, Zorena K, Semetkowska-Jurkiewicz E, Rachoń D, Suchanek H, et al. (2005) High levels of circulating interleukin-10 in diabetic nephropathy patients. Eur Cytokine Netw 16: 117-122.
75. Kalechman Y, Gafter U, Weinstein T, Chagnac A, Freidkin I, et al. (2004) Inhibition of interleukin-10 by the immunomodulator AS101 reduces mesangial cell proliferation in experimental mesangioproliferative glomerulonephritis: association with dephosphorylation of STAT3. J Biol Chem 279: 24724-24732.
76. Kalechman Y, Gafter U, Gal R, Rushkin G, Yan D, et al. (2002) Anti-IL-10 therapeutic strategy using the immunomodulator AS101 in protecting mice from sepsis-induced death: dependence on timing of immunomodulating intervention. J Immunol 169: 384-392.
77. Sinuani I, Beberashvili I, Averbukh Z, Sandbank J (2013) Role of IL-10 in the progression of kidney disease. World J Transplant 3(4):91-98.
78. Kitching AR, Katerelos M, Mudge SJ, Tipping PG, Power DA, et al. (2002) Interleukin-10 inhibits experimental mesangial proliferative glomerulonephritis. Clin Exp Immunol 128: 36-43.
79. Choi YK, Kim YJ, Park HS, Choi K, Paik SG, et al. (2003) Suppression of glomerulosclerosis by adenovirus-mediated IL-10 expression in the kidney. Gene Ther 10: 559-568.
80. Mu W, Ouyang X, Agarwal A, Zhang L, Long DA, et al. (2005) IL-10 suppresses chemokines, inflammation, and fibrosis in a model of chronic renal disease. J Am Soc Nephrol 16: 3651-3660.
81. Dahle MK, Øverland G, Myhre AE, Stuestøl JF, Hartung T, et al. (2004) The phosphatidylinositol 3 kinase/protein kinase B signaling pathway is activated by lipoteichoic acid and plays a role in Kupffer cell production of interleukin-6 (IL-6) and IL-10. Infect Immun 72: 5704-11.