Endothelial Nitric Oxide Synthase Reduces Crescentic and Necrotic Glomerular Lesions, Reactive Oxygen Production, and MCP1 Production in Murine Lupus Nephritis

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Gilkeson, Gary S ^a,b   Mashmoushi, Ahmad K ^a   Ruiz, Phillip ^c   Caza, Tiffany N ^d   Perl, Andras ^d   Oates, Jim C ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b RALPH H JOHNSON VA MEDICAL CENTER   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CHEMOKINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CATALYSIS; CD4+ T LYMPHOCYTE; CHRONIC INFLAMMATION; CONTROLLED STUDY; DEATH; DISEASE SEVERITY; ENZYME DEFICIENCY; ENZYME INHIBITION; GLOMERULOPATHY; HISTOPATHOLOGY; HYPERPOLARIZATION; IMMUNE COMPLEX DEPOSITION; INFLAMMATORY INFILTRATE; KIDNEY CORTEX; LUPUS ERYTHEMATOSUS NEPHRITIS; MITOCHONDRION; MITOCHONDRION HYPERPOLARIZATION; MOUSE; NECROTIC GLOMERULAR LESION; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN FUNCTION; PROTEIN URINE LEVEL; PROTEINURIA; RAPIDLY PROGRESSIVE GLOMERULONEPHRITIS; SURVIVAL; URINARY CAST; VASCULITIS;

ANIMALS; ANTIGEN-ANTIBODY COMPLEX; CALCIUM; CD4-POSITIVE T-LYMPHOCYTES; CHEMOKINE CCL2; COMPLEMENT SYSTEM PROTEINS; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION; KIDNEY GLOMERULUS; LUPUS NEPHRITIS; MALE; MICE; MICE, INBRED MRL LPR; MITOCHONDRIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PROTEINURIA; REACTIVE OXYGEN SPECIES;

ANIMALIA; MURINAE; MUS;

EID: 84878596635     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064650     Document Type: Article

References (43)

1. Crispin JC, Liossis SN, Kis-Toth K, Lieberman LA, Kyttaris VC, et al. (2010) Pathogenesis of human systemic lupus erythematosus: recent advances. Trends Mol Med 16: 47-57.
2. Sun Y, Oberley LW, (1996) Redox regulation of transcriptional activators. Free Radic Biol Med 21: 335-348.
3. Alderton WK, Cooper CE, Knowles RG, (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357: 593-615.
4. Oates JC The biology of reactive intermediates in systemic lupus erythematosus. Autoimmunity 43: 56-63.
5. El-Magadmi M, Bodill H, Ahmad Y, Durrington PN, Mackness M, et al. (2004) Systemic lupus erythematosus: an independent risk factor for endothelial dysfunction in women. Circulation 110: 399-404.
6. Furusu A, Miyazaki M, Abe K, Tsukasaki S, Shioshita K, et al. (1998) Expression of endothelial and inducible nitric oxide synthase in human glomerulonephritis. Kidney International 53: 1760-1768.
7. Bollain YGJJ, Ramirez-Sandoval R, Daza L, Esparza E, Barbosa O, et al. (2009) Widespread expression of inducible NOS and citrulline in lupus nephritis tissues. Inflammation Research 58: 61-66.
8. Chatterjee S, Ehrenshaft M, Bhattacharjee S, Deterding LJ, Bonini MG, et al. (2009) Immuno-spin trapping of a post-translational carboxypeptidase B1 radical formed by a dual role of xanthine oxidase and endothelial nitric oxide synthase in acute septic mice. Free Radic Biol Med 46: 454-461.
9. Nagy G, Barcza M, Gonchoroff N, Phillips PE, Perl A, (2004) Nitric oxide-dependent mitochondrial biogenesis generates Ca2+ signaling profile of lupus T cells. J Immunol 173: 3676-3683.
10. Njoku CJ, Patrick KS, Ruiz Jr P, Oates JC, (2005) Inducible nitric oxide synthase inhibitors reduce urinary markers of systemic oxidant stress in murine proliferative lupus nephritis. J Investig Med 53: 347-352.
11. Vyse TJ, Todd JA, (1996) Genetic analysis of autoimmune disease. Cell 85: 311-318.
12. Vidal S, Kono DH, Theofilopoulos AN, (1998) Loci predisposing to autoimmunity in MRL-Fas lpr and C57BL/6-Faslpr mice. J Clin Invest 101: 696-702.
13. Watson ML, Rao JK, Gilkeson GS, Ruiz P, Eicher EM, et al. (1992) Genetic analysis of MRL-lpr mice: relationship of the Fas apoptosis gene to disease manifestations and renal disease-modifying loci. Journal of Experimental Medicine 176: 1645-1656.
14. Njoku C, Self SE, Ruiz P, Hofbauer AF, Gilkeson GS, et al. (2008) Inducible nitric oxide synthase inhibitor SD-3651 reduces proteinuria in MRL/lpr mice deficient in the NOS2 gene. J Investig Med 56: 911-919.
15. Oates JC, Ruiz P, Alexander A, Pippen AM, Gilkeson GS, (1997) Effect of late modulation of nitric oxide production on murine lupus. Clin Immunol Immunopathol 83: 86-92.
16. Taylor TP, Janech MG, Slate EH, Lewis EC, Arthur JM, et al. (2012) Overcoming the effects of matrix interference in the measurement of urine protein analytes. Biomark Insights 7: 1-8.
17. Perl A, Nagy G, Gergely P, Puskas F, Qian Y, et al. (2004) Apoptosis and mitochondrial dysfunction in lymphocytes of patients with systemic lupus erythematosus. Methods Mol Med 102: 87-114.
18. Hagiwara M, Bledsoe G, Yang ZR, Smith RS Jr, Chao L, et al. (2008) Intermedin ameliorates vascular and renal injury by inhibition of oxidative stress. Am J Physiol Renal Physiol 295: F1735-1743.
19. Gupte SA, Levine RJ, Gupte RS, Young ME, Lionetti V, et al. (2006) Glucose-6-phosphate dehydrogenase-derived NADPH fuels superoxide production in the failing heart. J Mol Cell Cardiol 41: 340-349.
20. Nagy G, Perl A, (2006) The role of nitric oxide in abnormal T cell signal transduction in systemic lupus erythematosus. Clin Immunol 118: 145-151.
21. Marks SD, Williams SJ, Tullus K, Sebire NJ, (2008) Glomerular expression of monocyte chemoattractant protein-1 is predictive of poor renal prognosis in pediatric lupus nephritis. Nephrol Dial Transplant 23: 3521-3526.
22. Brunner HI, Bennett MR, Mina R, Suzuki M, Petri M, et al. (2012) Association of noninvasively measured renal protein biomarkers with histologic features of lupus nephritis. Arthritis & Rheumatism 64: 2687-2697.
23. Noris M, Bernasconi S, Casiraghi F, Sozzani S, Gotti E, et al. (1995) Monocyte chemoattractant protein-1 is excreted in excessive amounts in the urine of patients with lupus nephritis. Laboratory Investigation 73: 804-809.
24. Kulkarni O, Pawar RD, Purschke W, Eulberg D, Selve N, et al. (2007) Spiegelmer inhibition of CCL2/MCP-1 ameliorates lupus nephritis in MRL-(Fas)lpr mice. J Am Soc Nephrol 18: 2350-2358.
25. Volk T, Hensel M, Schuster H, Kox WJ, (2000) Secretion of MCP-1 and IL-6 by cytokine stimulated production of reactive oxygen species in endothelial cells. Mol Cell Biochem 206: 105-112.
26. Tsao PS, Wang B, Buitrago R, Shyy JY, Cooke JP, (1997) Nitric oxide regulates monocyte chemotactic protein-1. Circulation 96: 934-940.
27. Pober JS, Sessa WC, (2007) Evolving functions of endothelial cells in inflammation. Nat Rev Immunol 7: 803-815.
28. Schoeb TR, Jarmi T, Hicks MJ, Henke S, Zarjou A, et al. (2012) Endothelial nitric oxide synthase inhibits the development of autoimmune-mediated vasculitis in mice. Arthritis Rheum 64: 4114-4124.
29. Shah D, Wanchu A, Bhatnagar A, (2011) Interaction between oxidative stress and chemokines: possible pathogenic role in systemic lupus erythematosus and rheumatoid arthritis. Immunobiology 216: 1010-1017.
30. Kabe Y, Ando K, Hirao S, Yoshida M, Handa H, (2005) Redox regulation of NF-kappaB activation: distinct redox regulation between the cytoplasm and the nucleus. Antioxid Redox Signal 7: 395-403.
31. (2012) Champion ChiP Transcription Factor Search Portal.
32. Bendall JK, Alp NJ, Warrick N, Cai S, Adlam D, et al. (2005) Stoichiometric relationships between endothelial tetrahydrobiopterin, endothelial NO synthase (eNOS) activity, and eNOS coupling in vivo: insights from transgenic mice with endothelial-targeted GTP cyclohydrolase 1 and eNOS overexpression. Circ Res 97: 864-871.
33. Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, et al. (2003) Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 111: 1201-1209.
34. Moens AL, Kass DA, (2006) Tetrahydrobiopterin and cardiovascular disease. Arteriosclerosis, Thrombosis, and Vascular Biology 26: 2439-2444.
35. Fukai T, Siegfried MR, Ushio-Fukai M, Cheng Y, Kojda G, et al. (2000) Regulation of the vascular extracellular superoxide dismutase by nitric oxide and exercise training. Journal of Clinical Investigation 105: 1631-1639.
36. Bedard K, Krause KH, (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313.
37. Sumiyoshi K, Mokuno H, Iesaki T, Shimada K, Miyazaki T, et al. (2008) Deletion of the Fc receptors gamma chain preserves endothelial function affected by hypercholesterolaemia in mice fed on a high-fat diet. Cardiovasc Res 80: 463-470.
38. Stielow C, Catar RA, Muller G, Wingler K, Scheurer P, et al. (2006) Novel Nox inhibitor of oxLDL-induced reactive oxygen species formation in human endothelial cells. Biochem Biophys Res Commun 344: 200-205.
39. Selemidis S, Dusting GJ, Peshavariya H, Kemp-Harper BK, Drummond GR, (2007) Nitric oxide suppresses NADPH oxidase-dependent superoxide production by S-nitrosylation in human endothelial cells. Cardiovasc Res 75: 349-358.
40. Pleskova M, Beck KF, Behrens MH, Huwiler A, Fichtlscherer B, et al. (2006) Nitric oxide down-regulates the expression of the catalytic NADPH oxidase subunit Nox1 in rat renal mesangial cells. FASEB J 20: 139-141.
41. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, et al. (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 101: 2567-2578.
42. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, et al. (1996) Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 93: 13176-13181.
43. Kiss E, Soltesz P, Der H, Kocsis Z, Tarr T, et al. (2006) Reduced flow-mediated vasodilation as a marker for cardiovascular complications in lupus patients. Journal of Autoimmunity 27: 211-217.