An Endothelial Hsp70-TLR4 Axis Limits Nox3 Expression and Protects Against Oxidant Injury in Lungs

Antioxidants and Redox Signaling

Volumn 24, Issue 17, 2016, Pages 991-1012

  Zhang, Yi ^a   Shan, Peiying ^a   Srivastava, Anup ^a   Jiang, Ge ^a   Zhang, Xuchen ^a   Lee, Patty J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 70; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NOX3 PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STAT3 PROTEIN; SUPEROXIDE; SUPEROXIDE DISMUTASE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; NOX3 PROTEIN, MOUSE; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EOSINOPHIL; HYPEROXIA; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; LUNG ENDOTHELIUM; LUNG INJURY; LYMPHOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ACUTE LUNG INJURY; ANIMAL; BINDING SITE; C3H MOUSE; C57BL MOUSE; ENZYME REPRESSION; ENZYMOLOGY; GENE EXPRESSION; GENETICS; KNOCKOUT MOUSE; LUNG; LUNG ALVEOLUS EPITHELIUM CELL; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY; PROMOTER REGION; SIGNAL TRANSDUCTION;

ACUTE LUNG INJURY; ALVEOLAR EPITHELIAL CELLS; ANIMALS; APOPTOSIS; BASE SEQUENCE; BINDING SITES; ENZYME REPRESSION; GENE EXPRESSION; HSP70 HEAT-SHOCK PROTEINS; HYPEROXIA; LUNG; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; NADPH OXIDASE; PROMOTER REGIONS, GENETIC; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTOR 4;

EID: 84974809057     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2015.6505     Document Type: Article

References (38)

1. Banfi B, Malgrange B, Knisz J, Steger K, Dubois-Dauphin M, Krause KH. NOX3, a superoxide-generating NADPH oxidase of the inner ear. J Biol Chem 279: 46065-46072, 2004.
2. Benipal B, Feinstein SI, Chatterjee S, Dodia C, Fisher AB. Inhibition of the phospholipase A2 activity of peroxiredoxin 6 prevents lung damage with exposure to hyperoxia. Redox Biol 4: 321-327, 2015.
3. Cai H, Dikalov S, Griendling KK, Harrison DG. Detection of reactive oxygen species and nitric oxide in vascular cells and tissues: comparison of sensitivity and specificity. Methods Mol Med 139: 293-311, 2007.
4. Cantu E, Shah RJ, Lin W, Daye ZJ, Diamond JM, Suzuki Y, Ellis JH, Borders CF,ah GA, Beduhn B, Meyer NJ, Ruschefski M, Aplenc R, Feng R, Christie JD; Lung Transplant Outcomes Group I. Oxidant stress regulatory genetic variation in recipients and donors contributes to risk of primary graft dysfunction after lung transplantation. J Thorac Cardiovasc Surg 149: 596-602, 2015.
5. Cheng G, Cao Z, Xu X, van Meir EG, Lambeth JD. Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, Nox5. Gene 269: 131-140, 2001.
6. Dikalov SI and Harrison DG. Methods for detection of mitochondrial and cellular reactive oxygen species. Antioxid Redox Signal 20: 372-382, 2014.
7. Frame FM, Hager S, Pellacani D, Stower MJ, Walker HF, Burns JE, Collins AT, Maitland NJ. Development and limitations of lentivirus vectors as tools for tracking differentiation in prostate epithelial cells. Exp Cell Res 316: 3161-3171, 2010.
8. Gao D, Nong S, Huang X, Lu Y, Zhao H, Lin Y, Man Y, Wang S, Yang J, Li J. The effects of palmitate on hepatic insulin resistance are mediated by NADPH Oxidase 3-derived reactive oxygen species through JNK and p38MAPK pathways. J Biol Chem 285: 29965-29973, 2010.
9. Geiszt M and Leto TL. The Nox family of NAD(P)H oxidases: host defense and beyond. J Biol Chem 279: 51715-51718, 2004.
10. Hecker L, Logsdon NJ, Kurundkar D, Kurundkar A, Bernard K, Hock T, Meldrum E, Sanders YY, Thannickal VJ. Reversal of persistent fibrosis in aging by targeting Nox4-Nrf2 redox imbalance. Sci Transl Med 6: 231ra47, 2014.
11. Hunt CR, Dix DJ, Sharma GG, Pandita RK, Gupta A, Funk M, Pandita TK. Genomic instability and enhanced radiosensitivity in Hsp70.1-and Hsp70.3-deficient mice. Mol Cell Biol 24: 899-911, 2004.
12. Kano A, Wolfgang MJ, Gao Q, Jacoby J, Chai GX, Hansen W, Iwamoto Y, Pober JS, Flavell RA, Fu XY. Endothelial cells require STAT3 for protection against endotoxin-induced inflammation. J Exp Med 198: 1517-1525, 2003.
13. Konior A, Schramm A, Czesnikiewicz-Guzik M, Guzik TJ. NADPH oxidases in vascular pathology. Antioxid Redox Signal 20: 2794-2814, 2014.
14. Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4: 181-189, 2004.
15. Lambeth JD, Kawahara T, Diebold B. Regulation of Nox and Duox enzymatic activity and expression. Free Radic Biol Med 43: 319-331, 2007.
16. Liu X, Pei C, Yan S, Liu G, Liu G, Chen W, Cui Y, Liu Y. NADPH oxidase 1-dependent ROS is crucial for TLR4 signaling to promote tumor metastasis of non-small cell lung cancer. Tumour Biol 36: 1493-1502, 2015.
17. Montezano AC, Dulak-Lis M, Tsiropoulou S, Harvey A, Briones AM, Touyz RM. Oxidative stress and human hypertension: vascular mechanisms, biomarkers, novel therapies. Can J Cardiol 31: 631-641, 2015.
18. Morimoto H, Kanatsu-Shinohara M, Shinohara T. ROSgenerating oxidase Nox3 regulates the self-renewal of mouse spermatogonial stem cells. Biol Reprod 92: 147, 2015.
19. Paffenholz R, Bergstrom RA, Pasutto F, Wabnitz P, Munroe RJ, Jagla W, Heinzmann U, Marquardt A, Bareiss A, Laufs J, Russ A, Stumm G, Schimenti JC, Bergstrom DE. Vestibular defects in head-tilt mice result from mutations in Nox3, encoding an NADPH oxidase. Genes Dev 18: 486-491, 2004.
20. Park HS, Jung HY, Park EY, Kim J, Lee WJ, Bae YS. Cutting edge: direct interaction of TLR4 with NAD(P)H oxidase 4 isozyme is essential for lipopolysaccharide-induced production of reactive oxygen species and activation of NF-kappa B. J Immunol 173: 3589-3593, 2004.
21. Peshavariya HM, Dusting GJ, Selemidis S. Analysis of dihydroethidium fluorescence for the detection of intracellular and extracellular superoxide produced by NADPH oxidase. Free Radic Res 41: 699-712, 2007.
22. Qureshi ST, Zhang X, Aberg E, Bousette N, Giaid A, Shan P, Medzhitov RM, Lee PJ. Inducible activation of TLR4 confers resistance to hyperoxia-induced pulmonary apoptosis. J Immunol 176: 4950-4958, 2006.
23. Ruwanpura SM, McLeod L, Lilja AR, Brooks G, Dousha LF, Seow HJ, Bozinovski S, Vlahos R, Hertzog PJ,erson GP, Jenkins BJ. Non-essential role for TLR2 and its signaling adaptor Mal/TIRAP in preserving normal lung architecture in mice. PLoS One 8: e78095, 2013.
24. Rybak LP, Mukherjea D, Jajoo S, Kaur T, Ramkumar V. siRNA-mediated knock-down of NOX3: therapy for hearing loss? Cell Mol Life Sci 69: 2429-2434, 2012.
25. Sanders YY, Liu H, Liu G, Thannickal VJ. Epigenetic mechanisms regulate NADPH oxidase-4 expression in cellular senescence. Free Radic Biol Med 79: 197-205, 2015.
26. Siner JM, Jiang G, Cohen ZI, Shan P, Zhang X, Lee CG, Elias JA, Lee PJ. VEGF-induced heme oxygenase-1 confers cytoprotection from lethal hyperoxia in vivo. FASEB J 21: 1422-1432, 2007.
27. Stowe DF and Camara AK. Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid Redox Signal 11: 1373-1414, 2009.
28. Takyar S, Zhang Y, Haslip M, Jin L, Shan P, Zhang X, Lee PJ. An endothelial TLR4-VEGFR2 pathway mediates lung protection against oxidant-induced injury. FASEB J 30: 1317-1327, 2016.
29. Valente AJ, El Jamali A, Epperson TK, Gamez MJ, Pearson DW, Clark RA. NOX1 NADPH oxidase regulation by the NOXA1 SH3 domain. Free Radic Biol Med 43: 384-396, 2007.
30. Wojtala A, Bonora M, Malinska D, Pinton P, Duszynski J, Wieckowski MR. Methods to monitor ROS production by fluorescence microscopy and fluorometry. Methods Enzymol 542: 243-262, 2014.
31. Wu F, Szczepaniak WS, Shiva S, Liu H, Wang Y, Wang L, Wang Y, Kelley EE, Chen AF, Gladwin MT, McVerry BJ. Nox2-dependent glutathionylation of endothelial NOS leads to uncoupled superoxide production and endothelial barrier dysfunction in acute lung injury. Am J Physiol Lung Cell Mol Physiol 307: L987-L997, 2014.
32. Zhang X, Shan P, Jiang D, Noble PW, Abraham NG, Kappas A, Lee PJ. Small interfering RNA targeting heme oxygenase-1 enhances ischemia-reperfusion-induced lung apoptosis. J Biol Chem 279: 10677-10684, 2004.
33. Zhang X, Shan P, Jiang G, Cohn L, Lee PJ. Toll-like receptor 4 deficiency causes pulmonary emphysema. J Clin Invest 116: 3050-3059, 2006.
34. Zhang X, Shan P, Jiang G, Zhang SS, Otterbein LE, Fu XY, Lee PJ. Endothelial STAT3 is essential for the protective effects of HO-1 in oxidant-induced lung injury. FASEB J 20: 2156-2158, 2006.
35. Zhang X, Shan P, Qureshi S, Homer R, Medzhitov R, Noble PW, Lee PJ. Cutting edge: TLR4 deficiency confers susceptibility to lethal oxidant lung injury. J Immunol 175: 4834-4838, 2005.
36. Zhang Y, Jiang G, Sauler M, Lee PJ. Lung endothelial HO-1 targeting in vivo using lentiviral miRNA regulates apoptosis and autophagy during oxidant injury. FASEB J 27: 4041-4058, 2013.
37. Zhang Y, Sauler M, Shinn AS, Gong H, Haslip M, Shan P, Mannam P, Lee PJ. Endothelial PINK1 mediates the protective effects of NLRP3 deficiency during lethal oxidant injury. J Immunol 192: 5296-5304, 2014.
38. Zhang Y, Zhang X, Shan P, Hunt CR, Pandita TK, Lee PJ. A protective Hsp70-TLR4 pathway in lethal oxidant lung injury. J Immunol 191: 1393-1403, 2013.