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Published in: BMC Pulmonary Medicine 1/2019

Open Access 01-12-2019 | Idiopathic Pulmonary Fibrosis | Research article

The overexpression of peroxiredoxin-4 affects the progression of idiopathic pulmonary fibrosis

Authors: Tetsuya Hanaka, Takashi Kido, Shingo Noguchi, Sohsuke Yamada, Hirotsugu Noguchi, Xin Guo, Aya Nawata, Ke-Yong Wang, Keishi Oda, Tsutomu Takaki, Hiroto Izumi, Hiroshi Ishimoto, Kazuhiro Yatera, Hiroshi Mukae

Published in: BMC Pulmonary Medicine | Issue 1/2019

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Abstract

Background

Acute exacerbation of idiopathic pulmonary fibrosis (AE-IPF) is life-threatening. Several serum biomarkers, such as Krebs von den Lungen-6 (KL-6) and surfactant protein D (SP-D), are clinically used for evaluating AE-IPF, but these biomarkers are not adequate for establishing an early and accurate diagnosis of AE-IPF. Recently, the protective roles of the members of the peroxiredoxin (PRDX) family have been reported in IPF; however, the role of PRDX4 in AE-IPF is unclear.

Methods

Serum levels of PRDX4 protein, KL-6, SP-D and lactate dehydrogenase (LDH) in 51 patients with stable IPF (S-IPF), 38 patients with AE-IPF and 15 healthy volunteers were retrospectively assessed using enzyme-linked immunosorbent assay. Moreover, as an animal model of pulmonary fibrosis, wild-type (WT) and PRDX4-transgenic (Tg) mice were intratracheally administered with bleomycin (BLM, 2 mg/kg), and fibrotic and inflammatory changes in lungs were evaluated 3 weeks after the intratracheal administration.

Results

Serum levels of PRDX4 protein, KL-6, SP-D and LDH in patients with S-IPF and AE-IPF were significantly higher than those in healthy volunteers, and those in AE-IPF patients were the highest among the three groups. Using receiver operating characteristic curves, area under the curve values of serum PRDX4 protein, KL-6, SP-D, and LDH for detecting AE-IPF were 0.873, 0.698, 0.675, and 0.906, respectively. BLM-treated Tg mice demonstrated aggravated histopathological findings and poor prognosis compared with BLM-treated WT mice. Moreover, PRDX4 expression was observed in alveolar macrophages and lung epithelial cells of BLM-treated Tg mice.

Conclusions

PRDX4 is associated with the aggravation of inflammatory changes and fibrosis in the pathogenesis of IPF, and serum PRDX4 may be useful in clinical practice of IPF patients.
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Literature
1.
go back to reference Schaffer JM, Singh SK, Reitz BA, Zamanian RT, Mallidi HR. Single- vs double-lung transplantation in patients with chronic obstructive pulmonary disease and idiopathic pulmonary fibrosis since the implementation of lung allocation based on medical need. JAMA. 2015;313:936–48.PubMedCrossRef Schaffer JM, Singh SK, Reitz BA, Zamanian RT, Mallidi HR. Single- vs double-lung transplantation in patients with chronic obstructive pulmonary disease and idiopathic pulmonary fibrosis since the implementation of lung allocation based on medical need. JAMA. 2015;313:936–48.PubMedCrossRef
2.
go back to reference Rosas IO, Goldberg HJ, Collard HR, El-Chemaly S, Flaherty K, Hunninghake GM, et al. A phase II clinical trial of low-dose inhaled carbon monoxide in idiopathic pulmonary fibrosis. Chest. 2018;153:94–104.PubMedCrossRef Rosas IO, Goldberg HJ, Collard HR, El-Chemaly S, Flaherty K, Hunninghake GM, et al. A phase II clinical trial of low-dose inhaled carbon monoxide in idiopathic pulmonary fibrosis. Chest. 2018;153:94–104.PubMedCrossRef
3.
go back to reference du Bois RM. An earlier and more confident diagnosis of idiopathic pulmonary fibrosis. Eur Respir Rev. 2012;21:141–6.PubMedCrossRef du Bois RM. An earlier and more confident diagnosis of idiopathic pulmonary fibrosis. Eur Respir Rev. 2012;21:141–6.PubMedCrossRef
4.
go back to reference Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, et al. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med. 2011;183:788–824.PubMedPubMedCentralCrossRef Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, et al. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med. 2011;183:788–824.PubMedPubMedCentralCrossRef
5.
go back to reference Oda K, Yatera K, Fujino Y, Ishimoto H, Nakao H, Hanaka T, et al. Efficacy of concurrent treatments in idiopathic pulmonary fibrosis patients with a rapid progression of respiratory failure: an analysis of a national administrative database in Japan. BMC Pulm Med. 2016;16:91.PubMedPubMedCentralCrossRef Oda K, Yatera K, Fujino Y, Ishimoto H, Nakao H, Hanaka T, et al. Efficacy of concurrent treatments in idiopathic pulmonary fibrosis patients with a rapid progression of respiratory failure: an analysis of a national administrative database in Japan. BMC Pulm Med. 2016;16:91.PubMedPubMedCentralCrossRef
6.
go back to reference Juarez MM, Chan AL, Norris AG, Morrissey BM, Albertson TE. Acute exacerbation of idiopathic pulmonary fibrosis-a review of current and novel pharmacotherapies. J Thorac Dis. 2015;7:499–519.PubMedPubMedCentral Juarez MM, Chan AL, Norris AG, Morrissey BM, Albertson TE. Acute exacerbation of idiopathic pulmonary fibrosis-a review of current and novel pharmacotherapies. J Thorac Dis. 2015;7:499–519.PubMedPubMedCentral
7.
go back to reference Takahashi H, Fujishima T, Koba H, Murakami S, Kurokawa K, Shibuya Y, et al. Serum surfactant proteins a and D as prognostic factors in idiopathic pulmonary fibrosis and their relationship to disease extent. Am J Respir Crit Care Med. 2000;162:1109–14.PubMedCrossRef Takahashi H, Fujishima T, Koba H, Murakami S, Kurokawa K, Shibuya Y, et al. Serum surfactant proteins a and D as prognostic factors in idiopathic pulmonary fibrosis and their relationship to disease extent. Am J Respir Crit Care Med. 2000;162:1109–14.PubMedCrossRef
8.
go back to reference Ohnishi H, Yokoyama A, Kondo K, Hamada H, Abe M, Nishimura K, et al. Comparative study of KL-6, surfactant protein-a, surfactant protein-D, and monocyte chemoattractant protein-1 as serum markers for interstitial lung diseases. Am J Respir Crit Care Med. 2002;165:378–81.PubMedCrossRef Ohnishi H, Yokoyama A, Kondo K, Hamada H, Abe M, Nishimura K, et al. Comparative study of KL-6, surfactant protein-a, surfactant protein-D, and monocyte chemoattractant protein-1 as serum markers for interstitial lung diseases. Am J Respir Crit Care Med. 2002;165:378–81.PubMedCrossRef
9.
go back to reference Ohta S, Okamoto M, Fujimoto K, Sakamoto N, Takahashi K, Yamamoto H, et al. The usefulness of monomeric periostin as a biomarker for idiopathic pulmonary fibrosis. PLoS One. 2017;12:e0174547.PubMedPubMedCentralCrossRef Ohta S, Okamoto M, Fujimoto K, Sakamoto N, Takahashi K, Yamamoto H, et al. The usefulness of monomeric periostin as a biomarker for idiopathic pulmonary fibrosis. PLoS One. 2017;12:e0174547.PubMedPubMedCentralCrossRef
10.
go back to reference Kakugawa T, Yokota S, Ishimatsu Y, Hayashi T, Nakashima S, Hara S, et al. Serum heat shock protein 47 levels are elevated in acute exacerbation of idiopathic pulmonary fibrosis. Cell Stress Chaperones. 2013;18:581–90.PubMedPubMedCentralCrossRef Kakugawa T, Yokota S, Ishimatsu Y, Hayashi T, Nakashima S, Hara S, et al. Serum heat shock protein 47 levels are elevated in acute exacerbation of idiopathic pulmonary fibrosis. Cell Stress Chaperones. 2013;18:581–90.PubMedPubMedCentralCrossRef
11.
go back to reference Rhee SG, Chae HZ, Kim K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med. 2015;38:1543–52.CrossRef Rhee SG, Chae HZ, Kim K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med. 2015;38:1543–52.CrossRef
12.
go back to reference Kang SW, Rhee SG, Chang TS, Jeong W, Choi MH. 2-Cys peroxiredoxin function in intracellular signal transduction: therapeutic implications. Trends Mol Med. 2005;11:571–8.PubMedCrossRefPubMedCentral Kang SW, Rhee SG, Chang TS, Jeong W, Choi MH. 2-Cys peroxiredoxin function in intracellular signal transduction: therapeutic implications. Trends Mol Med. 2005;11:571–8.PubMedCrossRefPubMedCentral
13.
go back to reference Jin DY, Chae HZ, Rhee SG, Jeang KT. Regulatory role for a novel human thioredoxin peroxidase in NF-kappaB activation. J Biol Chem. 1997;272:30952–61.PubMedCrossRef Jin DY, Chae HZ, Rhee SG, Jeang KT. Regulatory role for a novel human thioredoxin peroxidase in NF-kappaB activation. J Biol Chem. 1997;272:30952–61.PubMedCrossRef
14.
go back to reference Giguere P, Turcotte ME, Hamelin E, Parent A, Brisson J, Laroche G, et al. Peroxiredoxin-4 interacts with and regulates the thromboxane a(2) receptor. FEBS Lett. 2007;581:3863–8.PubMedCrossRef Giguere P, Turcotte ME, Hamelin E, Parent A, Brisson J, Laroche G, et al. Peroxiredoxin-4 interacts with and regulates the thromboxane a(2) receptor. FEBS Lett. 2007;581:3863–8.PubMedCrossRef
15.
go back to reference Matsumoto A, Okado A, Fujii T, Fujii J, Egashira M, Niikawa N, et al. Cloning of the peroxiredoxin gene family in rats and characterization of the fourth member. FEBS Lett. 1999;443:246–50.PubMedCrossRef Matsumoto A, Okado A, Fujii T, Fujii J, Egashira M, Niikawa N, et al. Cloning of the peroxiredoxin gene family in rats and characterization of the fourth member. FEBS Lett. 1999;443:246–50.PubMedCrossRef
16.
go back to reference Kikuchi N, Ishii Y, Morishima Y, Yageta Y, Haraguchi N, Yamadori T, et al. Aggravation of bleomycin-induced pulmonary inflammation and fibrosis in mice lacking peroxiredoxin I. Am J Respir Cell Mol Biol. 2011;45:600–9.PubMedCrossRef Kikuchi N, Ishii Y, Morishima Y, Yageta Y, Haraguchi N, Yamadori T, et al. Aggravation of bleomycin-induced pulmonary inflammation and fibrosis in mice lacking peroxiredoxin I. Am J Respir Cell Mol Biol. 2011;45:600–9.PubMedCrossRef
17.
go back to reference Vuorinen K, Ohlmeier S, Leppäranta O, Salmenkivi K, Myllärniemi M, Kinnula VL. Peroxiredoxin II expression and its association with oxidative stress and cell proliferation in human idiopathic pulmonary fibrosis. J Histochem Cytochem. 2008;56:951–9.PubMedPubMedCentralCrossRef Vuorinen K, Ohlmeier S, Leppäranta O, Salmenkivi K, Myllärniemi M, Kinnula VL. Peroxiredoxin II expression and its association with oxidative stress and cell proliferation in human idiopathic pulmonary fibrosis. J Histochem Cytochem. 2008;56:951–9.PubMedPubMedCentralCrossRef
19.
go back to reference Guo X, Yamada S, Tanimoto A, Ding Y, Wang KY, Shimajiri S, et al. Overexpression of peroxiredoxin 4 attenuates atherosclerosis in apolipoprotein E knockout mice. Antioxid Redox Signal. 2012;17:1362–75.PubMedPubMedCentralCrossRef Guo X, Yamada S, Tanimoto A, Ding Y, Wang KY, Shimajiri S, et al. Overexpression of peroxiredoxin 4 attenuates atherosclerosis in apolipoprotein E knockout mice. Antioxid Redox Signal. 2012;17:1362–75.PubMedPubMedCentralCrossRef
20.
go back to reference Nawata A, Noguchi H, Mazaki Y, Kurahashi T, Izumi H, Wang KY, et al. Overexpression of peroxiredoxin 4 affects intestinal function in a dietary mouse model of nonalcoholic fatty liver disease. PLoS One. 2016;11:e0152549.PubMedPubMedCentralCrossRef Nawata A, Noguchi H, Mazaki Y, Kurahashi T, Izumi H, Wang KY, et al. Overexpression of peroxiredoxin 4 affects intestinal function in a dietary mouse model of nonalcoholic fatty liver disease. PLoS One. 2016;11:e0152549.PubMedPubMedCentralCrossRef
21.
go back to reference Collard HR, Moore BB, Flaherty KR, Brown KK, Kaner RJ, King TE Jr, et al. Acute exacerbations of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2007;176:636–43.PubMedCrossRef Collard HR, Moore BB, Flaherty KR, Brown KK, Kaner RJ, King TE Jr, et al. Acute exacerbations of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2007;176:636–43.PubMedCrossRef
22.
go back to reference Travis WD, Costabel U, Hansell DM, King TE Jr, Lynch DA, Nicholson AG, et al. An official American Thoracic Society/European Respiratory Society statement: update of the international multidisciplinary classification of the idiopathic interstitial pneumonias. Am J Respir Crit Care Med. 2013;188:733–48.PubMedPubMedCentralCrossRef Travis WD, Costabel U, Hansell DM, King TE Jr, Lynch DA, Nicholson AG, et al. An official American Thoracic Society/European Respiratory Society statement: update of the international multidisciplinary classification of the idiopathic interstitial pneumonias. Am J Respir Crit Care Med. 2013;188:733–48.PubMedPubMedCentralCrossRef
23.
go back to reference Ding Y, Yamada S, Wang KY, Shimajiri S, Guo X, Tanimoto A, et al. Overexpression of peroxiredoxin 4 protects against high-dose streptozotocin-induced diabetes by suppressing oxidative stress and cytokines in transgenic mice. Antioxid Redox Signal. 2010;13:1477–90.PubMedCrossRef Ding Y, Yamada S, Wang KY, Shimajiri S, Guo X, Tanimoto A, et al. Overexpression of peroxiredoxin 4 protects against high-dose streptozotocin-induced diabetes by suppressing oxidative stress and cytokines in transgenic mice. Antioxid Redox Signal. 2010;13:1477–90.PubMedCrossRef
24.
25.
go back to reference Nabeshima A, Yamada S, Guo X, Tanimoto A, Wang KY, Shimajiri S, et al. Peroxiredoxin 4 protects against nonalcoholic steatohepatitis and type 2 diabetes in a nongenetic mouse model. Antioxid Redox Signal. 2013;19:1983–98.PubMedPubMedCentralCrossRef Nabeshima A, Yamada S, Guo X, Tanimoto A, Wang KY, Shimajiri S, et al. Peroxiredoxin 4 protects against nonalcoholic steatohepatitis and type 2 diabetes in a nongenetic mouse model. Antioxid Redox Signal. 2013;19:1983–98.PubMedPubMedCentralCrossRef
26.
go back to reference Noguchi S, Yatera K, Wang KY, Oda K, Akata K, Yamasaki K, et al. Nitric oxide exerts protective effects against bleomycin-induced pulmonary fibrosis in mice. Respir Res. 2014;15:92.PubMedPubMedCentralCrossRef Noguchi S, Yatera K, Wang KY, Oda K, Akata K, Yamasaki K, et al. Nitric oxide exerts protective effects against bleomycin-induced pulmonary fibrosis in mice. Respir Res. 2014;15:92.PubMedPubMedCentralCrossRef
27.
go back to reference Noguchi H, Yamada S, Nabeshima A, Guo X, Tanimoto A, Wang KY, et al. Depletion of apoptosis signal-regulating kinase 1 prevents bile duct ligation-induced necroinflammation and subsequent peribiliary fibrosis. Am J Pathol. 2014;184:644–61.PubMedCrossRef Noguchi H, Yamada S, Nabeshima A, Guo X, Tanimoto A, Wang KY, et al. Depletion of apoptosis signal-regulating kinase 1 prevents bile duct ligation-induced necroinflammation and subsequent peribiliary fibrosis. Am J Pathol. 2014;184:644–61.PubMedCrossRef
28.
go back to reference Sakamoto N, Ishimatsu Y, Kakugawa T, Yura H, Tomonaga M, Harada T, et al. Elevated plasma alpha-defensins in patients with acute exacerbation of fibrotic interstitial pneumonia. Respir Med. 2015;109:265–71.PubMedCrossRef Sakamoto N, Ishimatsu Y, Kakugawa T, Yura H, Tomonaga M, Harada T, et al. Elevated plasma alpha-defensins in patients with acute exacerbation of fibrotic interstitial pneumonia. Respir Med. 2015;109:265–71.PubMedCrossRef
29.
go back to reference Ishizaka A, Matsuda T, Albertine KH, Koh H, Tasaka S, Hasegawa N, et al. Elevation of KL-6, a lung epithelial cell marker, in plasma and epithelial lining fluid in acute respiratory distress syndrome. Am J Physiol Lung Cell Mol Physiol. 2004;286:L1088–94.PubMedCrossRef Ishizaka A, Matsuda T, Albertine KH, Koh H, Tasaka S, Hasegawa N, et al. Elevation of KL-6, a lung epithelial cell marker, in plasma and epithelial lining fluid in acute respiratory distress syndrome. Am J Physiol Lung Cell Mol Physiol. 2004;286:L1088–94.PubMedCrossRef
30.
go back to reference Enomoto Y, Matsushima S, Shibata K, Aoshima Y, Yagi H, Meguro S, et al. LTBP2 is secreted from lung myofibroblasts and is a potential biomarker for idiopathic pulmonary fibrosis. Clin Sci (Lond). 2018;132:1565–80.CrossRef Enomoto Y, Matsushima S, Shibata K, Aoshima Y, Yagi H, Meguro S, et al. LTBP2 is secreted from lung myofibroblasts and is a potential biomarker for idiopathic pulmonary fibrosis. Clin Sci (Lond). 2018;132:1565–80.CrossRef
31.
go back to reference Hirasawa Y, Kohno N, Yokoyama A, Inoue Y, Abe M, Hiwada K. KL-6, a human MUC1 mucin, is chemotactic for human fibroblasts. Am J Respir Cell Mol Biol. 1997;17:501–7.PubMedCrossRef Hirasawa Y, Kohno N, Yokoyama A, Inoue Y, Abe M, Hiwada K. KL-6, a human MUC1 mucin, is chemotactic for human fibroblasts. Am J Respir Cell Mol Biol. 1997;17:501–7.PubMedCrossRef
32.
go back to reference Nickel CH, Ruedinger J, Misch F, Blume K, Maile S, Schulte J, et al. Copeptin and peroxiredoxin-4 independently predict mortality in patients with nonspecific complaints presenting to the emergency department. Acad Emerg Med. 2011;18:851–9.PubMedCrossRef Nickel CH, Ruedinger J, Misch F, Blume K, Maile S, Schulte J, et al. Copeptin and peroxiredoxin-4 independently predict mortality in patients with nonspecific complaints presenting to the emergency department. Acad Emerg Med. 2011;18:851–9.PubMedCrossRef
33.
go back to reference Schulte J, Struck J, Kohrle J, Muller B. Circulating levels of peroxiredoxin 4 as a novel biomarker of oxidative stress in patients with sepsis. Shock. 2011;35:460–5.PubMedCrossRef Schulte J, Struck J, Kohrle J, Muller B. Circulating levels of peroxiredoxin 4 as a novel biomarker of oxidative stress in patients with sepsis. Shock. 2011;35:460–5.PubMedCrossRef
34.
go back to reference Oku H, Shimizu T, Kawabata T, Nagira M, Hikita I, Ueyama A, et al. Antifibrotic action of pirfenidone and prednisolone: different effects on pulmonary cytokines and growth factors in bleomycin-induced murine pulmonary fibrosis. Eur J Pharmacol. 2008;590:400–8.PubMedCrossRef Oku H, Shimizu T, Kawabata T, Nagira M, Hikita I, Ueyama A, et al. Antifibrotic action of pirfenidone and prednisolone: different effects on pulmonary cytokines and growth factors in bleomycin-induced murine pulmonary fibrosis. Eur J Pharmacol. 2008;590:400–8.PubMedCrossRef
35.
go back to reference Wilson MS, Madala SK, Ramalingam TR, Gochuico BR, Rosas IO, Cheever AW, et al. Bleomycin and IL-1beta-mediated pulmonary fibrosis is IL-17A dependent. J Exp Med. 2010;207:535–52.PubMedPubMedCentralCrossRef Wilson MS, Madala SK, Ramalingam TR, Gochuico BR, Rosas IO, Cheever AW, et al. Bleomycin and IL-1beta-mediated pulmonary fibrosis is IL-17A dependent. J Exp Med. 2010;207:535–52.PubMedPubMedCentralCrossRef
36.
go back to reference Gasse P, Riteau N, Vacher R, Michel ML, Fautrel A, di Padova F, et al. IL-1 and IL-23 mediate early IL-17A production in pulmonary inflammation leading to late fibrosis. PLoS One. 2011;6:e23185.PubMedPubMedCentralCrossRef Gasse P, Riteau N, Vacher R, Michel ML, Fautrel A, di Padova F, et al. IL-1 and IL-23 mediate early IL-17A production in pulmonary inflammation leading to late fibrosis. PLoS One. 2011;6:e23185.PubMedPubMedCentralCrossRef
38.
go back to reference Shichita T, Hasegawa E, Kimura A, Morita R, Sakaguchi R, Takada I, et al. Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nat Med. 2012;18:911–7.PubMedCrossRef Shichita T, Hasegawa E, Kimura A, Morita R, Sakaguchi R, Takada I, et al. Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nat Med. 2012;18:911–7.PubMedCrossRef
39.
go back to reference Iwakura Y, Ishigame H, Saijo S, Nakae S. Functional specialization of interleukin-17 family members. Immun. 2011;34:149–62.CrossRef Iwakura Y, Ishigame H, Saijo S, Nakae S. Functional specialization of interleukin-17 family members. Immun. 2011;34:149–62.CrossRef
40.
go back to reference Kinnula VL, Fattman CL, Tan RJ, Oury TD. Oxidative stress in pulmonary fibrosis: a possible role for redox modulatory therapy. Am J Respir Crit Care Med. 2005;172:417–22.PubMedPubMedCentralCrossRef Kinnula VL, Fattman CL, Tan RJ, Oury TD. Oxidative stress in pulmonary fibrosis: a possible role for redox modulatory therapy. Am J Respir Crit Care Med. 2005;172:417–22.PubMedPubMedCentralCrossRef
41.
go back to reference Kuwano K, Nakashima N, Inoshima I, Hagimoto N, Fujita M, Yoshimi M, et al. Oxidative stress in lung epithelial cells from patients with idiopathic interstitial pneumonias. Eur Respir J. 2003;21:232–40.PubMedCrossRef Kuwano K, Nakashima N, Inoshima I, Hagimoto N, Fujita M, Yoshimi M, et al. Oxidative stress in lung epithelial cells from patients with idiopathic interstitial pneumonias. Eur Respir J. 2003;21:232–40.PubMedCrossRef
42.
go back to reference Wang Y, Feinstein SI, Manevich Y, Ho YS, Fisher AB. Peroxiredoxin 6 gene-targeted mice show increased lung injury with paraquat-induced oxidative stress. Antioxid Redox Signal. 2006;8:229–37.PubMedCrossRef Wang Y, Feinstein SI, Manevich Y, Ho YS, Fisher AB. Peroxiredoxin 6 gene-targeted mice show increased lung injury with paraquat-induced oxidative stress. Antioxid Redox Signal. 2006;8:229–37.PubMedCrossRef
43.
go back to reference Papiris SA, Tomos IP, Karakatsani A, Spathis A, Korbila I, Analitis A, et al. High levels of IL-6 and IL-8 characterize early-on idiopathic pulmonary fibrosis acute exacerbations. Cytokine. 2018;102:168–72.PubMedCrossRef Papiris SA, Tomos IP, Karakatsani A, Spathis A, Korbila I, Analitis A, et al. High levels of IL-6 and IL-8 characterize early-on idiopathic pulmonary fibrosis acute exacerbations. Cytokine. 2018;102:168–72.PubMedCrossRef
Metadata
Title
The overexpression of peroxiredoxin-4 affects the progression of idiopathic pulmonary fibrosis
Authors
Tetsuya Hanaka
Takashi Kido
Shingo Noguchi
Sohsuke Yamada
Hirotsugu Noguchi
Xin Guo
Aya Nawata
Ke-Yong Wang
Keishi Oda
Tsutomu Takaki
Hiroto Izumi
Hiroshi Ishimoto
Kazuhiro Yatera
Hiroshi Mukae
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Pulmonary Medicine / Issue 1/2019
Electronic ISSN: 1471-2466
DOI
https://doi.org/10.1186/s12890-019-1032-2

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