Endothelial nitric oxide synthase deficient mice are protected from lipopolysaccharide induced acute lung injury

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Gross, Christine M ^a   Rafikov, Ruslan ^a   Kumar, Sanjiv ^a   Aggarwal, Saurabh ^a   Ham, P Benson ^a   Meadows, Mary Louise ^a   Cherian Shaw, Mary ^a   Kangath, Archana ^a   Sridhar, Supriya ^a   Lucas, Rudolf ^a   Black, Stephen M ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMETHYLARGININASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EOTAXIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 9; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MYELOPEROXIDASE; PEROXYNITRITE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SUPEROXIDE; AMIDASE; CYTOKINE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA PROTEIN, MOUSE;

ACUTE LUNG INJURY; ADULT; AFFINITY CHROMATOGRAPHY; ANIMAL EXPERIMENT; ANIMAL HUSBANDRY; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; ENZYME SYNTHESIS; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LUNG COMPLIANCE; LUNG HEMODYNAMICS; LUNG LAVAGE; MALE; MOUSE; NITRATION; NONHUMAN; OXIDATIVE STRESS; OXYGEN SATURATION; ANIMAL; CHEMICALLY INDUCED; DEFICIENCY; KNOCKOUT MOUSE; LUNG FUNCTION TEST; METABOLISM;

MUS; NEGIBACTERIA;

ACUTE LUNG INJURY; AMIDOHYDROLASES; ANIMALS; CYTOKINES; LIPOPOLYSACCHARIDES; MICE; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE III; RESPIRATORY FUNCTION TESTS; RHO GTP-BINDING PROTEINS;

EID: 84925742271     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119918     Document Type: Article

References (74)

1. Ware LB, Matthay MA (2000) The acute respiratory distress syndrome. N Engl J Med 342: 1334-1349. PMID: 10793167
2. Bernard GR, Artigas A, Brigham KL, Carlet J, Falke K, Hudson L, et al. (1994) The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med 149: 818-824. PMID: 7509706
3. Lien E, Means TK, Heine H, Yoshimura A, Kusumoto S, Fukase K, et al. (2000) Toll-like receptor 4 imparts ligand-specific recognition of bacterial lipopolysaccharide. J Clin Invest 105: 497-504. PMID: 10683379
4. Kabir K, Gelinas JP, Chen M, Chen D, Zhang D, Luo X, et al. (2002) Characterization of a murine model of endotoxin-induced acute lung injury. Shock 17: 300-303. PMID: 11954830
5. Matthay MA, Ware LB, Zimmerman GA (2012) The acute respiratory distress syndrome. J Clin Invest 122: 2731-2740. doi: 10.1172/JCI60331 PMID: 22850883
6. Aggarwal S, Gross CM, Kumar S, Dimitropoulou C, Sharma S, Gorshkov BA, et al. (2014) Dimethylarginine dimethylaminohydrolase II overexpression attenuates LPS-mediated lung leak in acute lung injury. Am J Respir Cell Mol Biol 50: 614-625. doi: 10.1165/rcmb.2013-0193OC PMID: 24134589
7. Vallance P, Leone A, Calver A, Collier J, Moncada S (1992) Accumulation of an endogenous inhibitor of nitric oxide synthesis in chronic renal failure. Lancet 339: 572-575. PMID: 1347093
8. Druhan LJ, Forbes SP, Pope AJ, Chen CA, Zweier JL, Cardounel AJ (2008) Regulation of eNOS-derived superoxide by endogenous methylarginines. Biochemistry 47: 7256-7263. doi: 10.1021/bi702377a PMID: 18553936
9. Sud N, Wells SM, Sharma S, Wiseman DA, Wilham J, Black SM (2008) Asymmetric dimethylarginine inhibits HSP90 activity in pulmonary arterial endothelial cells: role of mitochondrial dysfunction. Am J Physiol Cell Physiol 294: C1407-1418. doi: 10.1152/ajpcell.00384.2007 PMID: 18385287
10. Wells SM, Holian A (2007) Asymmetric dimethylarginine induces oxidative and nitrosative stress in murine lung epithelial cells. Am J Respir Cell Mol Biol 36: 520-528. PMID: 17158357
11. Rafikov R, Dimitropoulou C, Aggarwal S, Kangath A, Gross C, Pardo D, et al. (2014) Lipopolysaccharide-induced lung injury involves the nitration-mediated activation of RhoA. J Biol Chem 289: 4710-4722. doi: 10.1074/jbc.M114.547596 PMID: 24398689
12. Boger RH (2004) Asymmetric dimethylarginine, an endogenous inhibitor of nitric oxide synthase, explains the "L-arginine paradox" and acts as a novel cardiovascular risk factor. J Nutr 134: 2842S-2847S; discussion 2853S. PMID: 15465797
13. Spindler V, Schlegel N, Waschke J (2010) Role of GTPases in control of microvascular permeability. Cardiovasc Res 87: 243-253. doi: 10.1093/cvr/cvq086 PMID: 20299335
14. Fagan KA, Tyler RC, Sato K, Fouty BW, Morris KG Jr., Huang PL, et al. (1999) Relative contributions of endothelial, inducible, and neuronal NOS to tone in the murine pulmonary circulation. Am J Physiol 277: L472-478. PMID: 10484454
15. Aggarwal S, Gross CM, Rafikov R, Kumar S, Fineman JR, Ludewig B, et al. (2014) Nitration of tyrosine 247 inhibits protein kinase G-1alpha activity by attenuating cyclic guanosine monophosphate binding. J Biol Chem 289: 7948-7961. doi: 10.1074/jbc.M113.534313 PMID: 24469460
16. Aggarwal S, Dimitropoulou C, Lu Q, Black SM, Sharma S (2012) Glutathione supplementation attenuates lipopolysaccharide-induced mitochondrial dysfunction and apoptosis in a mouse model of acute lung injury. Front Physiol 3: 161. doi: 10.3389/fphys.2012.00161 PMID: 22654772
17. Aggarwal S, Gross CM, Kumar S, Datar S, Oishi P, Kalkan G, et al. (2011) Attenuated vasodilatation in lambs with endogenous and exogenous activation of cGMP signaling: role of protein kinase G nitration. J Cell Physiol 226: 3104-3113. doi: 10.1002/jcp.22692 PMID: 21351102
18. Sharma S, Aramburo A, Rafikov R, Sun X, Kumar S, Oishi PE, et al. (2013) L-carnitine preserves endothelial function in a lamb model of increased pulmonary blood flow. Pediatr Res 74: 39-47. doi: 10. 1038/pr.2013.71 PMID: 23628882
19. Matute-Bello G, Winn RK, Jonas M, Chi EY, Martin TR, Liles WC (2001) Fas (CD95) induces alveolar epithelial cell apoptosis in vivo: implications for acute pulmonary inflammation. Am J Pathol 158: 153-161. PMID: 11141488
20. Sharma S, Smith A, Kumar S, Aggarwal S, Rehmani I, Snead C, et al. (2010) Mechanisms of nitric oxide synthase uncoupling in endotoxin-induced acute lung injury: role of asymmetric dimethylarginine. Vascul Pharmacol 52: 182-190. doi: 10.1016/j.vph.2009.11.010 PMID: 19962451
21. Arkovitz MS, Wispe JR, Garcia VF, Szabo C (1996) Selective inhibition of the inducible isoform of nitric oxide synthase prevents pulmonary transvascular flux during acute endotoxemia. J Pediatr Surg 31: 1009-1015. PMID: 8863222
22. Wei XQ, Charles IG, Smith A, Ure J, Feng GJ, Huang FP, et al. (1995) Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375: 408-411. PMID: 7539113
23. Kristof AS, Goldberg P, Laubach V, Hussain SN (1998) Role of inducible nitric oxide synthase in endotoxin-induced acute lung injury. Am J Respir Crit Care Med 158: 1883-1889. PMID: 9847282
24. Vromen A, Arkovitz MS, Zingarelli B, Salzman AL, Garcia VF, Szabo C (1996) Low-level expression and limited role for the inducible isoform of nitric oxide synthase in the vascular hyporeactivity and mortality associated with cecal ligation and puncture in the rat. Shock 6: 248-253. PMID: 8902940
25. Shelton JL, Wang L, Cepinskas G, Sandig M, Scott JA, North ML, et al. (2007) Inducible NO synthase (iNOS) in human neutrophils but not pulmonary microvascular endothelial cells (PMVEC) mediates septic protein leak in vitro. Microvasc Res 74: 23-31. PMID: 17451752
26. Ruetten H, Southan GJ, Abate A, Thiemermann C (1996) Attenuation of endotoxin-induced multiple organ dysfunction by 1-amino-2-hydroxy-guanidine, a potent inhibitor of inducible nitric oxide synthase. Br J Pharmacol 118: 261-270. PMID: 8735625
27. Kengatharan KM, De Kimpe SJ, Thiemermann C (1996) Role of nitric oxide in the circulatory failure and organ injury in a rodent model of gram-positive shock. Br J Pharmacol 119: 1411-1421. PMID: 8968550
28. De Kimpe SJ, Hunter ML, Bryant CE, Thiemermann C, Vane JR (1995) Delayed circulatory failure due to the induction of nitric oxide synthase by lipoteichoic acid from Staphylococcus aureus in anaesthetized rats. Br J Pharmacol 114: 1317-1323. PMID: 7542534
29. Koizumi T, Ogasawara H, Yamamato H, Tsushima K, Ruan Z, Jian M, et al. (2004) Effect of ONO1714, a specific inducible nitric oxide synthase inhibitor, on lung lymph filtration and gas exchange during endotoxemia in unanesthetized sheep. Anesthesiology 101: 59-65. PMID: 15220772
30. Laubach VE, Shesely EG, Smithies O, Sherman PA (1995) Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc Natl Acad Sci U S A 92: 10688-10692. PMID: 7479866
31. MacMicking JD, Nathan C, Hom G, Chartrain N, Fletcher DS, Trumbauer M, et al. (1995) Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81: 641-650. PMID: 7538909
32. Speyer CL, Neff TA, Warner RL, Guo RF, Sarma JV, Riedemann NC, et al. (2003) Regulatory effects of iNOS on acute lung inflammatory responses in mice. Am J Pathol 163: 2319-2328. PMID: 14633605
33. Hickey MJ, Sharkey KA, Sihota EG, Reinhardt PH, Macmicking JD, Nathan C, et al. (1997) Inducible nitric oxide synthase-deficient mice have enhanced leukocyte-endothelium interactions in endotoxemia. FASEB J 11: 955-964. PMID: 9337148
34. Zeidler PC, Millecchia LM, Castranova V (2004) Role of inducible nitric oxide synthase-derived nitric oxide in lipopolysaccharide plus interferon-gamma-induced pulmonary inflammation. Toxicol Appl Pharmacol 195: 45-54. PMID: 14962504
35. Lange M, Nakano Y, Traber DL, Hamahata A, Esechie A, Jonkam C, et al. (2010) Role of different nitric oxide synthase isoforms in a murine model of acute lung injury and sepsis. Biochem Biophys Res Commun 399: 286-291. doi: 10.1016/j.bbrc.2010.07.071 PMID: 20655878
36. Lange M, Hamahata A, Traber DL, Nakano Y, Traber LD, Enkhbaatar P (2011) Specific inhibition of nitric oxide synthases at different time points in a murine model of pulmonary sepsis. Biochem Biophys Res Commun 404: 877-881. doi: 10.1016/j.bbrc.2010.12.078 PMID: 21184738
37. Okamoto I, Abe M, Shibata K, Shimizu N, Sakata N, Katsuragi T, et al. (2000) Evaluating the role of inducible nitric oxide synthase using a novel and selective inducible nitric oxide synthase inhibitor in septic lung injury produced by cecal ligation and puncture. Am J Respir Crit Care Med 162: 716-722. PMID: 10934111
38. Lange M, Connelly R, Traber DL, Hamahata A, Cox RA, Nakano Y, et al. (2009) Combined neuronal and inducible nitric oxide synthase inhibition in ovine acute lung injury. Crit Care Med 37: 223-229. doi: 10.1097/CCM.0b013e3181926104 PMID: 19050630
39. Lange M, Hamahata A, Traber DL, Nakano Y, Esechie A, JonkamC, et al. (2010) Effects of early neuronal and delayed inducible nitric oxide synthase blockade on cardiovascular, renal, and hepatic function in ovine sepsis. Anesthesiology 113: 1376-1384. doi: 10.1097/ALN.0b013e3181fc5588 PMID: 21068663
40. Feletou M, Lonchampt M, Coge F, Galizzi JP, Bassoullet C, Merial C, et al. (2001) Regulation of murine airway responsiveness by endothelial nitric oxide synthase. Am J Physiol Lung Cell Mol Physiol 281: L258-267. PMID: 11404269
41. Miller AA, Hislop AA, Vallance PJ, Haworth SG (2005) Deletion of the eNOS gene has a greater impact on the pulmonary circulation of male than female mice. Am J Physiol Lung Cell Mol Physiol 289: L299-306. PMID: 15821017
42. Connelly L, Madhani M, Hobbs AJ (2005) Resistance to endotoxic shock in endothelial nitric-oxide synthase (eNOS) knock-out mice: a pro-inflammatory role for eNOS-derived no in vivo. J Biol Chem 280: 10040-10046. PMID: 15647265
43. Connelly L, Jacobs AT, Palacios-Callender M, Moncada S, Hobbs AJ (2003) Macrophage endothelial nitric-oxide synthase autoregulates cellular activation and pro-inflammatory protein expression. J Biol Chem 278: 26480-26487. PMID: 12740377
44. Vo PA, Lad B, Tomlinson JA, Francis S, Ahluwalia A (2005) autoregulatory role of endothelium-derived nitric oxide (NO) on Lipopolysaccharide-induced vascular inducible NO synthase expression and function. J Biol Chem 280: 7236-7243. PMID: 15583003
45. Fagan KA, Fouty BW, Tyler RC, Morris KG Jr., Hepler LK, Sato K, et al. (1999) The pulmonary circulation of homozygous or heterozygous eNOS-null mice is hyperresponsive to mild hypoxia. J Clin Invest 103: 291-299. PMID: 9916141
46. Steudel W, Ichinose F, Huang PL, Hurford WE, Jones RC, Bevan JA, et al. (1997) Pulmonary vasoconstriction and hypertension in mice with targeted disruption of the endothelial nitric oxide synthase (NOS 3) gene. Circ Res 81: 34-41. PMID: 9201025
47. Steudel W, Scherrer-Crosbie M, Bloch KD, Weimann J, Huang PL, Jones RC, et al. (1998) Sustained pulmonary hypertension and right ventricular hypertrophy after chronic hypoxia in mice with congenital deficiency of nitric oxide synthase 3. J Clin Invest 101: 2468-2477. PMID: 9616218
48. Han RN, Babaei S, Robb M, Lee T, Ridsdale R, Ackerley C, et al. (2004) Defective lung vascular development and fatal respiratory distress in endothelial NO synthase-deficient mice: a model of alveolar capillary dysplasia? Circ Res 94: 1115-1123. PMID: 15016731
49. Balasubramaniam V, Tang JR, Maxey A, Plopper CG, Abman SH (2003) Mild hypoxia impairs alveolarization in the endothelial nitric oxide synthase-deficient mouse. Am J Physiol Lung Cell Mol Physiol 284: L964-971. PMID: 12588707
50. Balasubramaniam V, Maxey AM, Morgan DB, Markham NE, Abman SH (2006) Inhaled NO restores lung structure in eNOS-deficient mice recovering from neonatal hypoxia. Am J Physiol Lung Cell Mol Physiol 291: L119-127. PMID: 16443642
51. Pheng LH, Francoeur C, Denis M (1995) The involvement of nitric oxide in a mouse model of adult respiratory distress syndrome. Inflammation 19: 599-610. PMID: 8543374
52. Iuvone T, D'Acquisto F, Carnuccio R, Di Rosa M (1996) Nitric oxide inhibits LPS-induced tumor necrosis factor synthesis in vitro and in vivo. Life Sci 59: PL207-211. PMID: 8809229
53. Bloomfield GL, Holloway S, Ridings PC, Fisher BJ, Blocher CR, Sholley M, et al. (1997) Pretreatment with inhaled nitric oxide inhibits neutrophil migration and oxidative activity resulting in attenuated sepsis-induced acute lung injury. Crit Care Med 25: 584-593. PMID: 9142021
54. Peng HB, Libby P, Liao JK (1995) Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B. J Biol Chem 270: 14214-14219. PMID: 7775482
55. Kubes P, Suzuki M, Granger DN (1991) Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci U S A 88: 4651-4655. PMID: 1675786
56. Ader F, Le Berre R, Lancel S, Faure K, Viget NB, Nowak E, et al. (2007) Inhaled nitric oxide increases endothelial permeability in Pseudomonas aeruginosa pneumonia. Intensive Care Med 33: 503-510. PMID: 17219196
57. Wu CH, Chen TL, Chen TG, Ho WP, Chiu WT, Chen RM (2003) Nitric oxide modulates pro- and anti-inflammatory cytokines in lipopolysaccharide-activated macrophages. J Trauma 55: 540-545. PMID: 14501900
58. Laszlo F, Whittle BJ, Evans SM, Moncada S (1995) Association of microvascular leakage with induction of nitric oxide synthase: effects of nitric oxide synthase inhibitors in various organs. Eur J Pharmacol 283: 47-53. PMID: 7498320
59. Peterson DA, Peterson DC, Archer S, Weir EK (1992) The non specificity of specific nitric oxide synthase inhibitors. Biochem Biophys Res Commun 187: 797-801. PMID: 1382421
60. Buxton IL, Cheek DJ, Eckman D, Westfall DP, Sanders KM, Keef KD (1993) NG-nitro L-arginine methyl ester and other alkyl esters of arginine are muscarinic receptor antagonists. Circ Res 72: 387-395. PMID: 7678206
61. Suda O, Tsutsui M, Morishita T, Tanimoto A, Horiuchi M, Tasaki H, et al. (2002) Long-term treatment with N(omega)-nitro-L-arginine methyl ester causes arteriosclerotic coronary lesions in endothelial nitric oxide synthase-deficient mice. Circulation 106: 1729-1735. PMID: 12270870
62. Suda O, Tsutsui M, Morishita T, Tasaki H, Ueno S, Nakata S, et al. (2004) Asymmetric dimethylarginine produces vascular lesions in endothelial nitric oxide synthase-deficient mice: involvement of reninangiotensin system and oxidative stress. Arterioscler Thromb Vasc Biol 24: 1682-1688. PMID: 15217805
63. Xia Y, Tsai AL, Berka V, Zweier JL (1998) Superoxide generation from endothelial nitric-oxide synthase. A Ca2+/calmodulin-dependent and tetrahydrobiopterin regulatory process. J Biol Chem 273: 25804-25808. PMID: 9748253
64. Xia Y, Dawson VL, Dawson TM, Snyder SH, Zweier JL (1996) Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc Natl Acad Sci U S A 93: 6770-6774. PMID: 8692893
65. Pou S, Pou WS, Bredt DS, Snyder SH, Rosen GM (1992) Generation of superoxide by purified brain nitric oxide synthase. J Biol Chem 267: 24173-24176. PMID: 1280257
66. Cardounel AJ, Cui H, Samouilov A, Johnson W, Kearns P, Tsai AL, et al. (2007) Evidence for the pathophysiological role of endogenous methylarginines in regulation of endothelial NO production and vascular function. J Biol Chem 282: 879-887. PMID: 17082183
67. Worrall NK, Chang K, LeJeune WS, Misko TP, Sullivan PM, Ferguson TB Jr., et al. (1997) TNF-alpha causes reversible in vivo systemic vascular barrier dysfunction via NO-dependent and-independent mechanisms. Am J Physiol 273: H2565-2574. PMID: 9435588
68. Leiper J, Murray-Rust J, McDonald N, Vallance P (2002) S-nitrosylation of dimethylarginine dimethylaminohydrolase regulates enzyme activity: further interactions between nitric oxide synthase and dimethylarginine dimethylaminohydrolase. Proc Natl Acad Sci U S A 99: 13527-13532. PMID: 12370443
69. Komarova Y, Malik AB (2010) Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu Rev Physiol 72: 463-493. doi: 10.1146/annurev-physiol-021909-135833 PMID: 20148685
70. Wojciak-Stothard B, Torondel B, Tsang LY, Fleming I, Fisslthaler B, Leiper JM, et al. (2007) The ADMA/DDAH pathway is a critical regulator of endothelial cell motility. J Cell Sci 120: 929-942. PMID: 17327280
71. Wojciak-Stothard B, Torondel B, Zhao L, Renne T, Leiper JM (2009) Modulation of Rac1 activity by ADMA/DDAH regulates pulmonary endothelial barrier function. Mol Biol Cell 20: 33-42. doi: 10.1091/mbc.E08-04-0395 PMID: 18923147
72. Qin L, Qin S, Zhang Y, Zhang C, Ma H, Li N, et al. (2014) p120 Modulates LPS-Induced NF- kappa B Activation Partially through RhoA in Bronchial Epithelial Cells. Biomed Res Int 2014: 932340. doi: 10.1155/2014/932340 PMID: 24995336
73. Perona R, Montaner S, Saniger L, Sanchez-Perez I, Bravo R, Lacal JC (1997) Activation of the nuclear factor-kappaB by Rho, CDC42, and Rac-1 proteins. Genes Dev 11: 463-475. PMID: 9042860
74. Yakovlev VA, Barani IJ, Rabender CS, Black SM, Leach JK, Graves PR, et al. (2007) Tyrosine nitration of IkappaBalpha: a novel mechanism for NF-kappaB activation. Biochemistry 46: 11671-11683. PMID: 17910475