Skip to main content
Top
Published in: Journal of Inflammation 1/2006

Open Access 01-12-2006 | Research

Migrating leukocytes are the source of Peroxiredoxin V during inflammation in the airways

Authors: Raisa I Krutilina, Andrei V Kropotov, Christian Leutenegger, Vladimir B Serikov

Published in: Journal of Inflammation | Issue 1/2006

Login to get access

Abstract

Background

We characterized changes in expression of the antioxidant protein Peroxiredoxin V (PRXV) during airway inflammation.

Methods

Studies in anesthetized rats and mice; PRXV expression determined by Western blot analyses and immunohistochemistry; PRXV m-RNA expression determined by Taq-Man RT-PCR.

Results

Bacterial lung inflammation did not change expression of PRXV in murine epithelia but produced massive influx of leukocytes highly expressing PRXV. Endotoxin and f-MLP induced leukocyte migration in rat trachea but did not change mRNA levels and PRXV protein expression in tracheal epithelial cells. In primary airway cell culture (cow), alveolar epithelial cells A549, or co-culture of A549 with murine macrophages RAW264.7, exposure to live bacteria increased expression of PRXV, which required serum. PRXV was secreted in vitro by epithelial and immune cells.

Conclusion

Inflammation increased expression of PRXV in airways by at least 2 mechanisms: cell population shift by massive influx of leukocytes expressing PRXV, and moderate post-transcriptional up-regulation of PRXV in epithelial cells.
Appendix
Available only for authorised users
Literature
1.
go back to reference Crapo JD: Redox active agents in inflammatory lung injury. Am J Resp Crit Care Med. 2003, 168: 1027-1028. 10.1164/rccm.2309001.PubMedCrossRef Crapo JD: Redox active agents in inflammatory lung injury. Am J Resp Crit Care Med. 2003, 168: 1027-1028. 10.1164/rccm.2309001.PubMedCrossRef
2.
go back to reference Kinnula VL: Focus on antioxidant enzymes and antioxidant strategies in smoking related airway diseases. Thorax. 2005, 60: 693-700. 10.1136/thx.2004.037473.PubMedPubMedCentralCrossRef Kinnula VL: Focus on antioxidant enzymes and antioxidant strategies in smoking related airway diseases. Thorax. 2005, 60: 693-700. 10.1136/thx.2004.037473.PubMedPubMedCentralCrossRef
3.
go back to reference Kinnula VL, Crapo JD: Superoxide dismutases in the lung and human lung diseases. Am J Resp Crit Care Med. 2003, 167: 1600-1619. 10.1164/rccm.200212-1479SO.PubMedCrossRef Kinnula VL, Crapo JD: Superoxide dismutases in the lung and human lung diseases. Am J Resp Crit Care Med. 2003, 167: 1600-1619. 10.1164/rccm.200212-1479SO.PubMedCrossRef
5.
go back to reference Kim HS, Kang SW, Rhee SG, Clerch LB: Rat lung peroxiredoxins I and II are differentially regulated during development and by hyperoxia. Am J Physiol Lung Cell Mol Physiol. 2001, 280: L1212-L1217.PubMed Kim HS, Kang SW, Rhee SG, Clerch LB: Rat lung peroxiredoxins I and II are differentially regulated during development and by hyperoxia. Am J Physiol Lung Cell Mol Physiol. 2001, 280: L1212-L1217.PubMed
6.
go back to reference Kinnula VL, Lehtonen S, Kaarteenaho-Wiik R, Lakari E, Paakko P, Kang SW, Rhee SG, Soini Y: Cell specific expression of peroxiredoxins in human lung and pulmonary sarcoidosis. Thorax. 2002, 57: 157-164. 10.1136/thorax.57.2.157.PubMedPubMedCentralCrossRef Kinnula VL, Lehtonen S, Kaarteenaho-Wiik R, Lakari E, Paakko P, Kang SW, Rhee SG, Soini Y: Cell specific expression of peroxiredoxins in human lung and pulmonary sarcoidosis. Thorax. 2002, 57: 157-164. 10.1136/thorax.57.2.157.PubMedPubMedCentralCrossRef
7.
go back to reference Manevich Y, Feinstein SI, Fisher AB: Activation of the antioxidant enzyme 1-CYS peroxiredoxin requires glutathionylation mediated by heterodimerization with GST. PNAS. 2004, 101: 3780-3785. 10.1073/pnas.0400181101.PubMedPubMedCentralCrossRef Manevich Y, Feinstein SI, Fisher AB: Activation of the antioxidant enzyme 1-CYS peroxiredoxin requires glutathionylation mediated by heterodimerization with GST. PNAS. 2004, 101: 3780-3785. 10.1073/pnas.0400181101.PubMedPubMedCentralCrossRef
8.
go back to reference Wang Y, Manevich Y, Feinstein SI, Fisher AB: Adenovirus-mediated transfer of the 1-cys peroxiredoxin gene to mouse lung protects against hyperoxic injury. Am J Physiol Lung Cell Mol Physiol. 2004, 286: L1188-L1193. 10.1152/ajplung.00288.2003.PubMedCrossRef Wang Y, Manevich Y, Feinstein SI, Fisher AB: Adenovirus-mediated transfer of the 1-cys peroxiredoxin gene to mouse lung protects against hyperoxic injury. Am J Physiol Lung Cell Mol Physiol. 2004, 286: L1188-L1193. 10.1152/ajplung.00288.2003.PubMedCrossRef
9.
go back to reference Yuan J, Murrell GAC, Trickett A, Landtmeters M, Knoops B, Wang M-X: Overexpression of antioxidant enzyme peroxiredoxin 5 protects human tendon cells against apoptosis and loss of cellular function during oxidative stress. Biochim et Biophys Acta – Mol Cell Res. 2004, 1693: 37-45. 10.1016/j.bbamcr.2004.04.006.CrossRef Yuan J, Murrell GAC, Trickett A, Landtmeters M, Knoops B, Wang M-X: Overexpression of antioxidant enzyme peroxiredoxin 5 protects human tendon cells against apoptosis and loss of cellular function during oxidative stress. Biochim et Biophys Acta – Mol Cell Res. 2004, 1693: 37-45. 10.1016/j.bbamcr.2004.04.006.CrossRef
10.
go back to reference Zhou Y, Kok KH, Chun AC, Wong CM, Wu HW, Lin MC, Fung PC, Kung H, Jin DY: Mouse peroxiredoxin V is a thioredoxin peroxidase that inhibits p53-induced apoptosis. Biochem Biophys Res Comm. 2000, 24: 921-927. 10.1006/bbrc.2000.2231.CrossRef Zhou Y, Kok KH, Chun AC, Wong CM, Wu HW, Lin MC, Fung PC, Kung H, Jin DY: Mouse peroxiredoxin V is a thioredoxin peroxidase that inhibits p53-induced apoptosis. Biochem Biophys Res Comm. 2000, 24: 921-927. 10.1006/bbrc.2000.2231.CrossRef
11.
go back to reference Kropotov AV, Grudinkin PS, Pleskach NM, Gavrilov BA, Tomilin NV, Zhivotovsky BD: Down-regulation of peroxiredoxin V stimulates formation of etoposide-induced double-strand DNA breaks. FEBS Letters. 2000, 572: 75-79. 10.1016/j.febslet.2004.07.011.CrossRef Kropotov AV, Grudinkin PS, Pleskach NM, Gavrilov BA, Tomilin NV, Zhivotovsky BD: Down-regulation of peroxiredoxin V stimulates formation of etoposide-induced double-strand DNA breaks. FEBS Letters. 2000, 572: 75-79. 10.1016/j.febslet.2004.07.011.CrossRef
12.
go back to reference Kropotov AV, Sedova V, Ivanov V, Sazeeva N, Tomilin A, Krutilina RI, Oei SL, Griesenbeck J, Buchlow G, Tomilin NV: A novel human DNA-binding protein with sequence similarity to a subfamily of redox proteins, which is able to repress RNA-polymerase-III-driven transcription of the Alu-family retroposons in vitro. Eur J Biochem. 1999, 260: 336-346. 10.1046/j.1432-1327.1999.00162.x.PubMedCrossRef Kropotov AV, Sedova V, Ivanov V, Sazeeva N, Tomilin A, Krutilina RI, Oei SL, Griesenbeck J, Buchlow G, Tomilin NV: A novel human DNA-binding protein with sequence similarity to a subfamily of redox proteins, which is able to repress RNA-polymerase-III-driven transcription of the Alu-family retroposons in vitro. Eur J Biochem. 1999, 260: 336-346. 10.1046/j.1432-1327.1999.00162.x.PubMedCrossRef
13.
go back to reference Kropotov AV, Tomilin NV: A human B-box-binding protein down-regulated in adenovirus 5-transformed human cells. FEBS Letters. 1996, 386: 43-46. 10.1016/0014-5793(96)00353-5.PubMedCrossRef Kropotov AV, Tomilin NV: A human B-box-binding protein down-regulated in adenovirus 5-transformed human cells. FEBS Letters. 1996, 386: 43-46. 10.1016/0014-5793(96)00353-5.PubMedCrossRef
14.
go back to reference Kropotov AV, Tomilin NV: Evidence for a regulatory protein complex on RNA polymerase III promoter of human retroposons of Alu family. Genetica. 1997, 98: 223-233. 10.1007/BF00057587.CrossRef Kropotov AV, Tomilin NV: Evidence for a regulatory protein complex on RNA polymerase III promoter of human retroposons of Alu family. Genetica. 1997, 98: 223-233. 10.1007/BF00057587.CrossRef
15.
go back to reference Serikov VB, Leutenegger C, Krutilina RI, Kropotov AV, Pleskach NM, Jung Suh, Tomilin NV: Cigarette Smoke Extract Inhibits Expression of Peroxiredoxin V and Increases Airway Epithelial Permeability. Inhalation Toxicology. 2006, 18: 79-92.PubMedCrossRef Serikov VB, Leutenegger C, Krutilina RI, Kropotov AV, Pleskach NM, Jung Suh, Tomilin NV: Cigarette Smoke Extract Inhibits Expression of Peroxiredoxin V and Increases Airway Epithelial Permeability. Inhalation Toxicology. 2006, 18: 79-92.PubMedCrossRef
16.
go back to reference Serikov VB, Popov BV, Kropotov AV, Tomilin NV: Bone Marrow-Derived Cells Restore Expression of Peroxiredoxin V in the Airways Following Acute Naphthalene Injury in Mice. Cytotherapy. 2005, 7: 483-493. 10.1080/14653240500361012.PubMedCrossRef Serikov VB, Popov BV, Kropotov AV, Tomilin NV: Bone Marrow-Derived Cells Restore Expression of Peroxiredoxin V in the Airways Following Acute Naphthalene Injury in Mice. Cytotherapy. 2005, 7: 483-493. 10.1080/14653240500361012.PubMedCrossRef
17.
go back to reference Knoops B, Clippe A, Bogard C, Arsalane K, Wattiez R, Hermans C, Duconseille E, Falmagne P, Bernard A: Cloning and characterization of AOEB166, a novel mammalian antioxidant enzyme of the peroxiredoxin family. J Biol Chem. 1999, 274: 30451-30458. 10.1074/jbc.274.43.30451.PubMedCrossRef Knoops B, Clippe A, Bogard C, Arsalane K, Wattiez R, Hermans C, Duconseille E, Falmagne P, Bernard A: Cloning and characterization of AOEB166, a novel mammalian antioxidant enzyme of the peroxiredoxin family. J Biol Chem. 1999, 274: 30451-30458. 10.1074/jbc.274.43.30451.PubMedCrossRef
18.
go back to reference Lehtonen ST, Markkanen PMH, Peltoniemi M, Sang Won Kang, Kinnula VL: Variable over-oxidation of peroxiredoxins in human lung cells in severe oxidative stress. Am J Physiol: Lung Cellular and Molecular Physiology. 2005, 288: L997-L1001. 10.1152/ajplung.00432.2004. Lehtonen ST, Markkanen PMH, Peltoniemi M, Sang Won Kang, Kinnula VL: Variable over-oxidation of peroxiredoxins in human lung cells in severe oxidative stress. Am J Physiol: Lung Cellular and Molecular Physiology. 2005, 288: L997-L1001. 10.1152/ajplung.00432.2004.
19.
go back to reference Serikov VB, Jang JY, Widdicombe JH: An estimate of hydrostatic pressure which drives fluid into airway lumen. J Appl Physiol. 2002, 92: 1702-1708.PubMedCrossRef Serikov VB, Jang JY, Widdicombe JH: An estimate of hydrostatic pressure which drives fluid into airway lumen. J Appl Physiol. 2002, 92: 1702-1708.PubMedCrossRef
20.
go back to reference Serikov VB, Choi H, Chmiel KJ, Wu R, Widdicombe JH: Role of ERK in the increase in airway epithelial permeability during leukocyte transmigration. Am J Resp Cell Mol Biol. 2004, 30: 261-270. 10.1165/rcmb.2003-0053OC.CrossRef Serikov VB, Choi H, Chmiel KJ, Wu R, Widdicombe JH: Role of ERK in the increase in airway epithelial permeability during leukocyte transmigration. Am J Resp Cell Mol Biol. 2004, 30: 261-270. 10.1165/rcmb.2003-0053OC.CrossRef
21.
go back to reference Lehtonen ST, Svensk AM, Soini Y, Paakko P, Hirvikoski P, Kang SW, Saily M, Kinnula VL: Peroxiredoxins, a novel protein family in lung cancer. Int J Cancer. 2004, 111: 514-21. 10.1002/ijc.20294.PubMedCrossRef Lehtonen ST, Svensk AM, Soini Y, Paakko P, Hirvikoski P, Kang SW, Saily M, Kinnula VL: Peroxiredoxins, a novel protein family in lung cancer. Int J Cancer. 2004, 111: 514-21. 10.1002/ijc.20294.PubMedCrossRef
22.
go back to reference Fajardo I, Svensson L, Bucht A, Pejler G: Increased levels of hypoxia-sensitive proteins in allergic airway inflammation. Am J Respir Crit Care Med. 2004, 170: 477-484. 10.1164/rccm.200402-178OC.PubMedCrossRef Fajardo I, Svensson L, Bucht A, Pejler G: Increased levels of hypoxia-sensitive proteins in allergic airway inflammation. Am J Respir Crit Care Med. 2004, 170: 477-484. 10.1164/rccm.200402-178OC.PubMedCrossRef
23.
go back to reference Das KC, Pahl PM, Guo XL, White CW: Induction of peroxiredoxin gene expression by oxygen in lungs of newborn primates. Am J Respir Cell Mol Biol. 2001, 25: 226-232.PubMedCrossRef Das KC, Pahl PM, Guo XL, White CW: Induction of peroxiredoxin gene expression by oxygen in lungs of newborn primates. Am J Respir Cell Mol Biol. 2001, 25: 226-232.PubMedCrossRef
24.
go back to reference Tomoaki Hoshino, Hajime Nakamura, Masaki Okamoto, Seiya Kato, Shinichi Araya, Keiko Nomiyama, Kotaro Oizumi, Young HA, Hisamichi Aizawa, Junji Yodoi: Redox-reactive protein Thioredoxin prevents proinflammatory cytokine- or Bleomycin-induced lung injury. Am J Resp and Crit Care Medicine. 2003, 168: 1075-1083. 10.1164/rccm.200209-982OC.CrossRef Tomoaki Hoshino, Hajime Nakamura, Masaki Okamoto, Seiya Kato, Shinichi Araya, Keiko Nomiyama, Kotaro Oizumi, Young HA, Hisamichi Aizawa, Junji Yodoi: Redox-reactive protein Thioredoxin prevents proinflammatory cytokine- or Bleomycin-induced lung injury. Am J Resp and Crit Care Medicine. 2003, 168: 1075-1083. 10.1164/rccm.200209-982OC.CrossRef
Metadata
Title
Migrating leukocytes are the source of Peroxiredoxin V during inflammation in the airways
Authors
Raisa I Krutilina
Andrei V Kropotov
Christian Leutenegger
Vladimir B Serikov
Publication date
01-12-2006
Publisher
BioMed Central
Published in
Journal of Inflammation / Issue 1/2006
Electronic ISSN: 1476-9255
DOI
https://doi.org/10.1186/1476-9255-3-13

Other articles of this Issue 1/2006

Journal of Inflammation 1/2006 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.