Peroxiredoxin i null mice exhibits reduced acute lung inflammation following ozone exposure

Journal of Biochemistry

Volumn 152, Issue 6, 2012, Pages 595-601

  Yanagisawa, Rie ^a   Warabi, Eiji ^b   Inoue, Ken Ichiro ^c   Yanagawa, Toru ^b   Koike, Eiko ^a   Ichinose, Takamichi ^d   Takano, Hirohisa ^a,e   Ishii, Tetsuro ^b  

^a NATIONAL INSTITUTE FOR ENVIRONMENTAL STUDIES   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c INTERNATIONAL UNIVERSITY OF HEALTH AND WELFARE   (Japan)

^d OITA UNIVERSITY OF NURSING AND HEALTH SCIENCES   (Japan)

^e KYOTO UNIVERSITY   (Japan)

Author keywords

acute lung inflammation; IL 6; KC; ozone; peroxiredoxin I

Indexed keywords

HEME OXYGENASE 1; MESSENGER RNA; OZONE; PEROXIREDOXIN 1;

ACUTE LUNG INJURY; AIR POLLUTANT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; INFLAMMATION; LUNG DISEASE; LUNG LAVAGE; MALE; MICROSCOPY; MOUSE; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ACUTE DISEASE; ANIMALS; GLUTATHIONE TRANSFERASE; HEME OXYGENASE-1; INFLAMMATION MEDIATORS; ISOENZYMES; LUNG; MACROPHAGES; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; NF-E2-RELATED FACTOR 2; OZONE; PEROXIREDOXINS; PNEUMONIA; RNA, MESSENGER; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

MUS;

EID: 84870865760     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvs113     Document Type: Article

References (42)

1. Bhalla, D.K. (1999) Ozone-induced lung inflammation and mucosal barrier disruption: toxicology, mechanisms, and implications. J. Toxicol. Environ. Health B Crit. Rev. 2, 31-86
2. Galan, I., Tobias, A., Banegas, J.R., and Aranguez, E. (2003) Short-term effects of air pollution on daily asthma emergency room admissions. Eur. Respir. J. 22, 802-808
3. Medina-Ramon, M., Zanobetti, A., and Schwartz, J. (2006) The effect of ozone and PM10 on hospital admissions for pneumonia and chronic obstructive pulmonary disease: a national multicity study. Am. J. Epidemiol. 163, 579-588
4. Tolbert, P.E., Mulholland, J.A., MacIntosh, D.L., Xu, F., Daniels, D., Devine, O.J., Carlin, B.P., Klein, M., Dorley, J., Butler, A.J., Nordenberg, D.F., Frumkin, H., Ryan, P.B., and White, M.C. (2000) Air quality and pediatric emergency room visits for asthma in Atlanta, Georgia, USA. Am. J. Epidemiol. 151, 798-810
5. Hollingsworth, J.W., Maruoka, S., Li, Z., Potts, E.N., Brass, D.M., Garantziotis, S., Fong, A., Foster, W.M., and Schwartz, D.A. (2007) Ambient ozone primes pulmonary innate immunity in mice. J. Immunol. 179, 4367-4375
6. Ballinger, C.A., Cueto, R., Squadrito, G., Coffin, J.F., Velsor, L.W., Pryor, W.A., and Postlethwait, E.M. (2005) Antioxidant-mediated augmentation of ozoneinduced membrane oxidation. Free Radic. Biol. Med. 38, 515-526
7. Ghio, A.J., Turi, J.L., Madden, M.C., Dailey, L.A., Richards, J.D., Stonehuerner, J.G., Morgan, D.L., Singleton, S., Garrick, L.M., and Garrick, M.D. (2007) Lung injury after ozone exposure is iron dependent. Am. J. Physiol. Lung Cell. Mol. Physiol. 292, L134-L143
8. Pryor, W.A. (1994) Mechanisms of radical formation from reactions of ozone with target molecules in the lung. Free Radic. Biol. Med. 17, 451-465
9. Kafoury, R.M., Pryor, W.A., Squadrito, G.L., Salgo, M.G., Zou, X., and Friedman, M. (1999) Induction of inflammatory mediators in human airway epithelial cells by lipid ozonation products. Am. J. Respir. Crit. Care Med. 160, 1934-1942
10. Mudway, I.S. and Kelly, F.J. (2000) Ozone and the lung: a sensitive issue. Mol. Aspects Med. 21, 1-48
11. Samet, J.M., Noah, T.L., Devlin, R.B., Yankaskas, J.R., McKinnon, K., Dailey, L.A., and Friedman, M. (1992) Effect of ozone on platelet-activating factor production in phorbol-differentiated HL60 cells, a human bronchial epithelial cell line (BEAS S6), and primary human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 7, 514-522
12. Kosmider, B., Loader, J.E., Murphy, R.C., and Mason, R.J. (2010) Apoptosis induced by ozone and oxysterols in human alveolar epithelial cells. Free Radic. Biol. Med. 48, 1513-1524
13. Ishii, T., Itoh, K., Takahashi, S., Sato, H., Yanagawa, T., Katoh, Y., Bannai, S., and Yamamoto, M. (2000) Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J. Biol. Chem. 275, 16023-16029
14. Ishii, T., Yamada, M., Sato, H., Matsue, M., Taketani, S., Nakayama, K., Sugita, Y., and Bannai, S. (1993) Cloning and characterization of a 23-kDa stress-induced mouse peritoneal macrophage protein. J. Biol. Chem. 268, 18633-18636
15. Ishii, T., Itoh, K., Ruiz, E., Leake, D.S., Unoki, H., Yamamoto, M., and Mann, G.E. (2004) Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal. Circ. Res. 94, 609-616
16. Hollingsworth, J.W., Kleeberger, S.R., and Foster, W.M. (2007) Ozone and pulmonary innate immunity. Proc. Am. Thorac. Soc. 4, 240-246
17. Kleeberger, S.R., Reddy, S., Zhang, L.Y., and Jedlicka, A.E. (2000) Genetic susceptibility to ozone-induced lung hyperpermeability: role of toll-like receptor 4. Am. J. Respir. Cell Mol. Biol. 22, 620-627
18. Kleeberger, S.R., Reddy, S.P., Zhang, L.Y., Cho, H.Y., and Jedlicka, A.E. (2001) Toll-like receptor 4 mediates ozone-induced murine lung hyperpermeability via inducible nitric oxide synthase. Am. J. Physiol. Lung Cell Mol. Physiol. 280, L326-L333
19. Hollingsworth, J.W. 2nd, Cook, D.N., Brass, D.M., Walker, J.K., Morgan, D.L., Foster, W.M., and Schwartz, D.A. (2004) The role of Toll-like receptor 4 in environmental airway injury in mice. Am. J. Respir. Crit. Care Med. 170, 126-132
20. Williams, A.S., Leung, S.Y., Nath, P., Khorasani, N.M., Bhavsar, P., Issa, R., Mitchell, J.A., Adcock, I.M., and Chung, K.F. (2007) Role of TLR2, TLR4, and MyD88 in murine ozone-induced airway hyperresponsiveness and neutrophilia. J. Appl. Physiol. 103, 1189-1195
21. Garantziotis, S., Li, Z., Potts, E.N., Lindsey, J.Y., Stober, V.P., Polosukhin, V.V., Blackwell, T.S., Schwartz, D.A., Foster, W.M., and Hollingsworth, J.W. (2010) TLR4 is necessary for hyaluronan-mediated airway hyperresponsiveness after ozone inhalation. Am. J. Respir. Crit. Care Med. 181, 666-675
22. Jiang, D., Liang, J., Fan, J., Yu, S., Chen, S., Luo, Y., Prestwich, G.D., Mascarenhas, M.M., Garg, H.G., Quinn, D.A., Homer, R.J., Goldstein, D.R., Bucala, R., Lee, P.J., Medzhitov, R., and Noble, P.W. (2005) Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat. Med. 11, 1173-1179
23. Taylor, K.R., Yamasaki, K., Radek, K.A., Di Nardo, A., Goodarzi, H., Golenbock, D., Beutler, B., and Gallo, R.L. (2007) Recognition of hyaluronan released in sterile injury involves a unique receptor complex dependent on Toll-like receptor 4, CD44, and MD-2. J. Biol. Chem. 282, 18265-18275
24. Rhee, S.G., Chae, H.Z., and Kim, K. (2005) Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 38, 1543-1552
25. Sato, D., Yanaka, A., Shibahara, T., Matsui, H., Nakahara, A., Yanagawa, T., Warabi, E., Ishii, T., and Hyodo, I. (2008) Peroxiredoxin I protects gastric mucosa from oxidative injury induced by H. pylori infection. J. Gastroenterol. Hepatol. 23, 652-659
26. Uwayama, J., Hirayama, A., Yanagawa, T., Warabi, E., Sugimoto, R., Itoh, K., Yamamoto, M., Yoshida, H., Koyama, A., and Ishii, T. (2006) Tissue Prx I in the protection against Fe-NTA and the reduction of nitroxyl radicals. Biochem. Biophys. Res. Commun. 339, 226-231
27. Kikuchi, N., Ishii, Y., Morishima, Y., Yageta, Y., Haraguchi, N., Yamadori, T., Masuko, H., Sakamoto, T., Yanagawa, T., Warabi, E., Ishii, T., and Hizawa, N. (2011) Aggravation of bleomycin-induced pulmonary inflammation and fibrosis in mice lacking peroxiredoxin I. Am. J. Respir. Cell Mol. Biol. 45, 600-609
28. Ishii, T., Warabi, E., and Yanagawa, T. (2012) Novel roles of peroxiredoxins in inflammation, cancer and innate immunity. J. Clin. Biochem. Nutr. 50, 91-105
29. Borch, J., Axelstad, M., Vinggaard, A.M., and Dalgaard, M. (2006) Diisobutyl phthalate has comparable anti-androgenic effects to di-n-butyl phthalate in fetal rat testis. Toxicol. Lett. 163, 183-190
30. Catterall, J.B., Rowan, A.D., Sarsfield, S., Saklatvala, J., Wait, R., and Cawston, T.E. (2006) Development of a novel 2D proteomics approach for the identification of proteins secreted by primary chondrocytes after stimulation by IL-1 and oncostatin M. Rheumatology (Oxford) 45, 1101-1109
31. Riddell, J.R., Wang, X.Y., Minderman, H., and Gollnick, S.O. (2010) Peroxiredoxin 1 stimulates secretion of proinflammatory cytokines by binding to TLR4. J. Immunol. 184, 1022-1030
32. Inoue, K., Takano, H., Koike, E., Warabi, E., Yanagawa, T., Yanagisawa, R., and Ishii, T. (2009) Peroxiredoxin I is a negative regulator of Th2-dominant allergic asthma. Int. Immunopharmacol. 9, 1281-1288
33. Shichita, T., Hasegawa, E., Kimura, A., Morita, R., Sakaguchi, R., Takada, I., Sekiya, T., Ooboshi, H., Kitazono, T., Yanagawa, T., Ishii, T., Takahashi, H., Mori, S., Nishibori, M., Kuroda, K., Akira, S., Miyake, K., and Yoshimura, A. (2012) Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nat. Med. 18, 911-917
34. Garcia-Bonilla, L. and Iadecola, C. (2012) Peroxiredoxin sets the brain on fire after stroke. Nat. Med. 18, 858-859
35. Kinnula, V.L., Lehtonen, S., Kaarteenaho-Wiik, R., Lakari, E., Paakko, P., Kang, S.W., Rhee, S.G., and Soini, Y. (2002) Cell specific expression of peroxiredoxins in human lung and pulmonary sarcoidosis. Thorax 57, 157-164
36. Zambrowicz, B.P., Friedrich, G.A., Buxton, E.C., Lilleberg, S.L., Person, C., and Sands, A.T. (1998) Disruption and sequence identification of 2,000 genes in mouse embryonic stem cells. Nature 392, 608-611
37. Blackwell, T.S., Blackwell, T.R., Holden, E.P., Christman, B.W., and Christman, J.W. (1996) In vivo antioxidant treatment suppresses nuclear factor-kappa B activation and neutrophilic lung inflammation. J. Immunol. 157, 1630-1637
38. Yanagisawa, R., Takano, H., Inoue, K., Ichinose, T., Yoshida, S., Sadakane, K., Takeda, K., Yoshino, S., Yamaki, K., Kumagai, Y., and Yoshikawa, T. (2004) Complementary DNA microarray analysis in acute lung injury induced by lipopolysaccharide and diesel exhaust particles. Exp. Biol. Med. (Maywood) 229, 1081-1087
39. Gharib, S.A., Nguyen, E., Altemeier, W.A., Shaffer, S.A., Doneanu, C.E., Goodlett, D.R., and Schnapp, L.M. (2010) Of mice and men: comparative proteomics of bronchoalveolar fluid. Eur. Respir. J. 35, 1388-1395
40. Guo, Y., Ma, S.F., Grigoryev, D., Van Eyk, J., and Garcia, J.G. (2005) 1-DE MS and 2-D LC-MS analysis of the mouse bronchoalveolar lavage proteome. Proteomics 5, 4608-4624
41. Geiben-Lynn, R., Kursar, M., Brown, N.V., Addo, M.M., Shau, H., Lieberman, J., Luster, A.D., and Walker, B.D. (2003) HIV-1 antiviral activity of recombinant natural killer cell enhancing factors, NKEF-A and NKEF-B, members of the peroxiredoxin family. J. Biol. Chem. 278, 1569-1574
42. Cho, H.Y., Morgan, D.L., Bauer, A.K., and Kleeberger, S.R. (2007) Signal transduction pathways of tumor necrosis factor-mediated lung injury induced by ozone in mice. Am. J. Respir. Crit. Care Med. 175, 829-839