DOI QR코드

DOI QR Code

Multiple Roles of Peroxiredoxins in Inflammation

  • Knoops, Bernard (Group of Animal Molecular and Cellular Biology, Institut des Sciences de la Vie (ISV), Universite catholique de Louvain) ;
  • Argyropoulou, Vasiliki (Group of Animal Molecular and Cellular Biology, Institut des Sciences de la Vie (ISV), Universite catholique de Louvain) ;
  • Becker, Sarah (Group of Animal Molecular and Cellular Biology, Institut des Sciences de la Vie (ISV), Universite catholique de Louvain) ;
  • Ferte, Laura (Group of Animal Molecular and Cellular Biology, Institut des Sciences de la Vie (ISV), Universite catholique de Louvain) ;
  • Kuznetsova, Oksana (Group of Animal Molecular and Cellular Biology, Institut des Sciences de la Vie (ISV), Universite catholique de Louvain)
  • 투고 : 2015.12.08
  • 심사 : 2015.12.11
  • 발행 : 2016.01.31

초록

Inflammation is a pathophysiological response to infection or tissue damage during which high levels of reactive oxygen and nitrogen species are produced by phagocytes to kill microorganisms. Reactive oxygen and nitrogen species serve also in the complex regulation of inflammatory processes. Recently, it has been proposed that peroxiredoxins may play key roles in innate immunity and inflammation. Indeed, peroxiredoxins are evolutionarily conserved peroxidases able to reduce, with high rate constants, hydrogen peroxide, alkyl hydroperoxides and peroxynitrite which are generated during inflammation. In this minireview, we point out different possible roles of peroxiredoxins during inflammatory processes such as cytoprotective enzymes against oxidative stress, modulators of redox signaling, and extracellular pathogen- or damage-associated molecular patterns. A better understanding of peroxiredoxin functions in inflammation could lead to the discovery of new therapeutic targets.

키워드

참고문헌

  1. Abbas, K., Breton, J., Picot, C.R., Quesniaux, V., Bouton, C., and Drapier, J.-C. (2009). Signaling events leading to peroxiredoxin 5 up-regulation in immunostimulated macrophages. Free Radic. Biol. Med. 47, 794-802. https://doi.org/10.1016/j.freeradbiomed.2009.06.018
  2. Adimora, N.J., Jones, D.P., and Kemp, M.L. (2010). A model of redox kinetics implicates the thiol proteome in cellular hydrogen peroxide responses. Antioxid. Redox Signal. 13, 731-743. https://doi.org/10.1089/ars.2009.2968
  3. Ahn, H.M., Lee, K.S., Lee, D.S., and Yu, K. (2012). JNK/FOXO mediated PeroxiredoxinV expression regulates redox homeostasis during Drosophila melanogaster gut infection. Dev. Comp. Immunol. 38, 466-473. https://doi.org/10.1016/j.dci.2012.07.002
  4. Bast, A., Erttmann, S.F., Walther, R., and Steinmetz, I. (2010). Influence of iNOS and COX on peroxiredoxin gene expression in primary macrophages. Free Radic. Biol. Med. 49, 1881-1891. https://doi.org/10.1016/j.freeradbiomed.2010.09.015
  5. Chae, H.Z., Chung, S.J., and Rhee, S.G. (1994). Thioredoxindependent peroxide reductase from yeast. J. Biol. Chem. 269, 27670-27678.
  6. Chatterjee, S., Feinstein, S.I., Dodia, C., Sorokina, E., Lien, Y.-C., Nguyen, S., Debolt, K., Speicher, D., and Fisher, A.B. (2011). Peroxiredoxin 6 phosphorylation and subsequent phospholipase A2 activity are required for agonist-mediated activation of NADPH oxidase in mouse pulmonary microvascular endothelium and alveolar macrophages. J. Biol. Chem. 286, 11696-11706. https://doi.org/10.1074/jbc.M110.206623
  7. Chen, H., Yin, Y., Feng, E., Li, Y., Xie, X., and Wang, Z. (2014). Thioredoxin peroxidase gene is involved in resistance to biocontrol fungus Nomuraea rileyi in Spodoptera litura: gene cloning, expression, localization and function. Dev. Comp. Immunol. 44, 76-85. https://doi.org/10.1016/j.dci.2013.11.012
  8. Choi, H.-I., Chung, K.-J., Yang, H.-Y., Ren, L., Sohn, S., Kim, P.-R., Kook, M.-S., Choy, H.E., and Lee, T.-H. (2013). Peroxiredoxin V selectively regulates IL-6 production by modulating the Jak2-Stat5 pathway. Free Radic. Biol. Med. 65, 270-279. https://doi.org/10.1016/j.freeradbiomed.2013.06.038
  9. Cox, A.G., Winterbourn, C.C. and Hampton, M.B. (2010). Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem. J. 425, 313-325. https://doi.org/10.1042/BJ20091541
  10. Desaint, S., Luriau, S., Aude, J.C., Rousselet, G., and Toledano, M.B. (2004). Mammalian antioxidant defenses are not inducible by $H_2O_2$. J. Biol. Chem. 279, 31157-31163. https://doi.org/10.1074/jbc.M401888200
  11. Diet, A., Abbas, K., Bouton, C., Guillon, B., Tomasello, F., Fourquet, S., Toledano, M.B., and Drapier, J.-C. (2007). Regulation of peroxiredoxins by nitric oxide in immunostimulated macrophages. J. Biol. Chem. 282, 36199-36205. https://doi.org/10.1074/jbc.M706420200
  12. Ding, Y., Yamada, S., Wang, K.-Y., Shimajiri, S., Guo, X., Tanimoto, A., Murata, Y., Kitajima, S., Watanabe, T., Izumi, H., et al. (2010). Overexpression of peroxiredoxin 4 protects against high-dose streptozotocin-induced diabetes by suppressing oxidative stress and cytokines in transgenic mice. Antioxid. Redox Signal. 13, 1477-1490. https://doi.org/10.1089/ars.2010.3137
  13. Donnelly, S., O'Neill, S.M., Sekiya, M., Mulcahy, G., and Dalton, J.P. (2005). Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infect. Immun. 73, 166-173. https://doi.org/10.1128/IAI.73.1.166-173.2005
  14. Donnelly, S., Stack, C.M., O'Neill, S.M., Sayed, A.A., Williams, D.L., and Dalton, J.P. (2008). Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages. FASEB J. 22, 4022-4032. https://doi.org/10.1096/fj.08-106278
  15. Ferrer-Sueta, G., Manta, B., Botti, H., Radi, R., Trujillo, M., and Denicola, A. (2011). Factors affecting protein thiol reactivity and specificity in peroxide reduction. Chem. Res. Toxicol. 24, 434-450. https://doi.org/10.1021/tx100413v
  16. Furuta, T., Imajo-Ohmi, S., Fukuda, H., Kano, S., Miyake, K., and Watanabe, N. (2008). Mast cell-mediated immune responses through IgE antibody and Toll-like receptor 4 by malarial peroxiredoxin. Eur. J. Immunol. 38, 1341-1350. https://doi.org/10.1002/eji.200738059
  17. Genard, B., Miner, P., Nicolas, J.L., Moraga, D., Boudry, P., Pernet, F., and Tremblay, R. (2013). Integrative study of physiological changes associated with bacterial infection in Pacific oyster larvae. PLoS One 8, e64534. https://doi.org/10.1371/journal.pone.0064534
  18. Gretes, M.C., Poole, L.B., and Karplus, P.A. (2012). Peroxiredoxins in parasites. Antioxid. Redox Signal. 17, 608-633. https://doi.org/10.1089/ars.2011.4404
  19. Hall, A., Parsonage, D., Poole, L.B., and Karplus, P.A. (2010). Structural evidence that peroxiredoxin catalytic power is based on transition-state stabilization. J. Mol. Biol. 402, 194-209. https://doi.org/10.1016/j.jmb.2010.07.022
  20. Hanschmann, E.-M., Godoy, J.R., Berndt, C., Hudemann, C., and Lillig, H.C. (2013). Thioredoxins, glutaredoxins, and peroxiredoxins-Molecular mechanisms and health significance:from cofactors to antioxidants to redox signaling. Antioxid. Redox Signal. 19, 1539-1605. https://doi.org/10.1089/ars.2012.4599
  21. Hofmann, B., Hecht, H.-J. and Flohe, L. (2002). Peroxiredoxins. Biol. Chem. 383, 347-364.
  22. Ishii, T. (2015). Close teamwork between Nrf2 and peroxiredoxins 1 and 6 for the regulation of prostaglandin D2 and E2 production in macrophages in acute inflammation. Free Radic. Biol. Med. 88, 189-198. https://doi.org/10.1016/j.freeradbiomed.2015.04.034
  23. 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. https://doi.org/10.3164/jcbn.11-109
  24. Kikuchi, N., Ishii, Y., Morishima, Y., Yageta, Y., Haraguchi, N., Yamadori, T., Masuko, H., Sakamoto, T., Yanagawa, T., Warabi, E., et al. (2011). Aggravation of bleomycin-induced pulmonary inflammation and fibrosis in mice lacking peroxiredoxin I. Am. J. Respir. Cell Mol. Biol. 45, 600-609. https://doi.org/10.1165/rcmb.2010-0137OC
  25. Kim, K., Kim, I.H., Lee, K.Y., Rhee, S.G. and Stadtman, E.R. (1988). The isolation and purification of a specific "protector" protein which inhibits enzyme inactivation by a Thiol/Fe(III)/O2 mixedfunction oxidation system. J. Biol. Chem. 263, 4704-4711.
  26. Kim, S.-U., Hwang, C.N., Sun, H.-N., Jin, M.-H., Han, Y.-H., Lee, H., Kim, J.-M., Kim, S.-K., Yu, D.-Y., Lee, D.-S., et al. (2008). Peroxiredoxin I is an indicator of microglia activation and protects against hydrogen peroxide-mediated microglial death. Biol. Pharm. Bull. 31, 820-825. https://doi.org/10.1248/bpb.31.820
  27. Kim, S.U., Park, Y.H., Min, J.S., Sun, H.N., Han, Y.H., Hua, J.M., Lee, T.H., Lee, S.R., Chang, K.T., Kang, S.W., et al. (2013). Peroxiredoxin I is a ROS/p38 MAPK-dependent inducible antioxidant that regulates NF-${\kappa}B$-mediated iNOS induction and microglial activation. J. Neuroimmunol. 259, 26-36. https://doi.org/10.1016/j.jneuroim.2013.03.006
  28. 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. https://doi.org/10.1136/thorax.57.2.157
  29. Knoops, B., Clippe, A., Bogard, C., Arsalane, K., Wattiez, R., Hermans, C., Duconseille, E., Falmagne, P., and Bernard, A. (1999). Cloning and characterization of AOEB166, a novel mammalian antioxidant enzyme of the peroxiredoxin family. J. Biol. Chem. 274, 30451-30458. https://doi.org/10.1074/jbc.274.43.30451
  30. Knoops, B., Loumaye, E., and Van Der Eecken, V. (2007). Evolution of peroxiredoxins. Subcell. Biochem. 44, 27-40. https://doi.org/10.1007/978-1-4020-6051-9_2
  31. Leyens, G., Donnay, I., and Knoops, B. (2003). Cloning of bovine peroxiredoxins-gene expression in bovine tissues and amino acid sequence comparison with rat, mouse and primate peroxiredoxins. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 136, 943-955. https://doi.org/10.1016/S1096-4959(03)00290-2
  32. Li, L., Shoji, W., Takano, H., Nishimura, N., Aoki, Y., Takahashi, R., Goto, S., Kaifu, T., Takai, T., and Obinata, M. (2007). Increased susceptibility of MER5 (peroxiredoxin III) knockout mice to LPSinduced oxidative stress. Biochem. Biophys. Res. Commun. 355, 715-721. https://doi.org/10.1016/j.bbrc.2007.02.022
  33. Mittal, M., Siddiqui, M.R., Tran, K., Reddy, S.P., and Malik, A.B. (2014). Reactive oxygen species in inflammation and tissue injury. Antioxid. Redox Signal. 20, 1126-1167. https://doi.org/10.1089/ars.2012.5149
  34. Mullen, L., Hanschmann, E.M., Lillig, C.H., Herzenberg, L.A., and Ghezzi, P. (2015). Cysteine oxidation targets peroxiredoxin 1 and 2 for exosomal release through a novel mechanism of redox-dependent secretion. Mol. Med. 21, 98-108. https://doi.org/10.1007/s00894-015-2638-9
  35. Nabeshima, A., Yamada, S., Guo, X., Tanimoto, A., Wang, K.Y., Shimajiri, S., Kimura, S., Tasaki, T., Noguchi, H., Kitada, S., et al. (2013). Peroxiredoxin 4 protects against nonalcoholic steatohepatitis and type 2 diabetes in a nongenetic mouse model. Antioxid. Redox Signal. 19, 1983-1998. https://doi.org/10.1089/ars.2012.4946
  36. Nathan, C., and Cunningham-Bussel, A. (2013). Beyond oxidative stress: an immunologist's guide to reactive oxygen species. Nat. Rev. Immunol. 13, 349-361. https://doi.org/10.1038/nri3423
  37. Nelson, K.J., Knutson, S.T., Soito, L., Klomsiri, C., Poole, L.B., and Fetrow, J.S. (2011). Analysis of the peroxiredoxin family: Using active-site structure and sequence information for global classification and residue analysis. Proteins 79, 947-964. https://doi.org/10.1002/prot.22936
  38. Newton, K., and Dixit, V.M. (2012). Signaling in innate immunity and inflammation. Cold Spring Harb. Perspect. Biol. 4, a006049.
  39. Perkins, A., Nelson, K.J., Parsonage, D., Poole, L.B., and Karplus, P.A. (2015). Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling. Trends Biochem. Sci. 40, 435-445. https://doi.org/10.1016/j.tibs.2015.05.001
  40. Portillo-Ledesma, S., Sardi, F., Manta, B., Tourn, M.V., Clippe, A., Knoops, B., Alvarez, B., Coitino, E.L., and Ferrer-Sueta, G. (2014). Deconstructing the catalytic efficiency of peroxiredoxin-5 peroxidatic cysteine. Biochemistry 53, 6113-6125. https://doi.org/10.1021/bi500389m
  41. Radyuk, S.N., Michalak, K., Klichko, V.I., Benes, J., Rebrin, I., Sohal, R.S., and Orr, W.C. (2009). Peroxiredoxin 5 confers protection against oxidative stress and apoptosis and also promotes longevity in Drosophila. Biochem. J. 419, 437-445. https://doi.org/10.1042/BJ20082003
  42. Radyuk, S.N., Michalak, K., Klichko, V.I., Benes, J., and Orr, W.C. (2010). Peroxiredoxin 5 modulates immune response in Drosophila. Biochim. Biophys. Acta 1800, 1153-1163. https://doi.org/10.1016/j.bbagen.2010.06.010
  43. Ren, L., Sun, Y., Wang, R., and Xu, T. (2014). Gene structure, immune response and evolution: comparative analysis of three 2-Cys peroxiredoxin members of miiuy croaker, Miichthys miiuy. Fish Shellfish Immunol. 36, 409-416. https://doi.org/10.1016/j.fsi.2013.12.014
  44. Rhee, S., and Woo, H. (2011). Multiple functions of peroxiredoxins:peroxidases, sensors and regulators of the intracellular messenger $H_2O_2$, and protein chaperones. Antioxid. Redox Signal. 15, 781-794. https://doi.org/10.1089/ars.2010.3393
  45. Rhee, S.G., Chae, H.Z., and Kim, K. (2005a). Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 38, 1543-1552. https://doi.org/10.1016/j.freeradbiomed.2005.02.026
  46. Rhee, S.G., Kang, S.W., Jeong, W., Chang, T.-S., Yang, K.-S., and Woo, H.A. (2005b). Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr. Opin. Cell Biol. 17, 183-189. https://doi.org/10.1016/j.ceb.2005.02.004
  47. 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. https://doi.org/10.4049/jimmunol.0901945
  48. Robinson, M.W., Hutchinson, A.T., Dalton, J.P., and Donnelly, S. (2010a). Peroxiredoxin: A central player in immune modulation. Parasite Immunol. 32, 305-313. https://doi.org/10.1111/j.1365-3024.2010.01201.x
  49. Robinson, M.W., Hutchinson, A.T., Donnelly, S., and Dalton, J.P. (2010b). Worm secretory molecules are causing alarm. Trends Parasitol. 26, 371-372. https://doi.org/10.1016/j.pt.2010.05.004
  50. Royet, J., Reichhart, J.M., and Hoffmann, J.A. (2005). Sensing and signaling during infection in Drosophila. Curr. Opin. Immunol. 17, 11-17. https://doi.org/10.1016/j.coi.2004.12.002
  51. Salzano, S., Checconi, P., Hanschmann, E.-M., Lillig, C.H., Bowler, L.D., Chan, P., Vaudry, D., Mengozzi, M., Coppo, L., Sacre, S., et al. (2014). Linkage of inflammation and oxidative stress via release of glutathionylated peroxiredoxin-2, which acts as a danger signal. Proc. Natl. Acad. Sci. USA. 111, 12157-12162. https://doi.org/10.1073/pnas.1401712111
  52. Seo, M.S., Kang, S.W., Kim, K., Baines, I.C., Lee, T.H., and Rhee, S.G. (2000). Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J. Biol. Chem. 275, 20346-20354. https://doi.org/10.1074/jbc.M001943200
  53. Shau, H., Gupta, R.K., and Golub, S.H. (1993). Identification of a natural killer enhancing factor (NKEF) from human erythroid cells. Cell. Immunol. 147, 1-11. https://doi.org/10.1006/cimm.1993.1043
  54. Shichita, T., Hasegawa, E., Kimura, A., Morita, R., Sakaguchi, R., Takada, I., Sekiya, T., Ooboshi, H., Kitazono, T., Yanagawa, T., et al. (2012). Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nat. Med. 18, 911-917. https://doi.org/10.1038/nm.2749
  55. Sies, H. (2014). Role of Metabolic $H_2O_2$ Generation: redox signaling and oxidative stress. J. Biol. Chem. 289, 8735-8741. https://doi.org/10.1074/jbc.R113.544635
  56. Sobotta, M.C., Liou, W., Stocker, S., Talwar, D., Oehler, M., Ruppert, T., Scharf, A.N., and Dick, T.P. (2015). Peroxiredoxin-2 and STAT3 form a redox relay for $H_2O_2$ signaling. Nat. Chem. Biol. 11, 64-70. https://doi.org/10.1038/nchembio.1695
  57. Sun, H.N., Kim, S.U., Huang, S.M., Kim, J.M., Park, Y.H., Kim, S.H., Yang, H.Y., Chung, K.J., Lee, T.H., Choi, H.S., et al. (2010). Microglial peroxiredoxin v acts as an inducible anti-inflammatory antioxidant through cooperation with redox signaling cascades. J. Neurochem. 114, 39-50.
  58. Valero, Y., Martinez-Morcillo, F.J., Esteban, M.A., Chaves-Pozo, E., and Cuesta, A. (2015). Fish peroxiredoxins and their role in immunity. Biology 4, 860-880. https://doi.org/10.3390/biology4040860
  59. Wang, M.-X., Wei, A., Yuan, J., Trickett, A., Knoops, B., and Murrell, G.A. (2002). Expression and regulation of peroxiredoxin 5 in human osteoarthritis. FEBS Lett. 531, 359-362. https://doi.org/10.1016/S0014-5793(02)03511-1
  60. Woo, H.A, Yim, S.H., Shin, D.H., Kang, D., Yu, D.Y., and Rhee, S.G. (2010). Inactivation of peroxiredoxin I by phosphorylation allows localized $H_2O_2$ accumulation for cell signaling. Cell. 140, 517-528. https://doi.org/10.1016/j.cell.2010.01.009
  61. Wood, Z. a, Schroder, E., Robin Harris, J. and Poole, L.B. (2003). Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28, 32-40. https://doi.org/10.1016/S0968-0004(02)00003-8
  62. Yang, C.-S., Lee, D.-S., Song, C.-H., An, S.-J., Li, S., Kim, J.-M., Kim, C.S., Yoo, D.G., Jeon, B.H., Yang, H.-Y., et al. (2007). Roles of peroxiredoxin II in the regulation of proinflammatory responses to LPS and protection against endotoxin-induced lethal shock. J. Exp. Med. 204, 583-594. https://doi.org/10.1084/jem.20061849
  63. Yu, S.H., Mu, Y.N., Ao, J.Q., and Chen, X.H. (2010). Peroxiredoxin IV regulates pro-inflammatory responses in large yellow croaker (Pseudosciaena crocea) and protects against bacterial challenge. J. Proteome Res. 9, 1424-1436. https://doi.org/10.1021/pr900961x
  64. Yun, H., Park, K., Kim, E., and Hong, J.T. (2015). PRDX6 controls multiple sclerosis by suppressing inflammation and blood brain barrier disruption. Oncotarget 6, 20875-20884. https://doi.org/10.18632/oncotarget.5205
  65. Zhang, L., and Lu, Z. (2015). Expression, purification and characterization of an atypical 2-Cys peroxiredoxin from the silkworm, Bombyx mori. Insect Mol. Biol. 24, 203-212. https://doi.org/10.1111/imb.12149

피인용 문헌

  1. The role of peroxiredoxin 6 in neutralization of X-ray mediated oxidative stress: effects on gene expression, preservation of radiosensitive tissues and postradiation survival of animals vol.51, pp.2, 2017, https://doi.org/10.1080/10715762.2017.1289377
  2. Cellular mechanisms of peroxynitrite-induced neuronal death vol.133, 2017, https://doi.org/10.1016/j.brainresbull.2017.05.008
  3. Formation and processing of DNA damage substrates for the hNEIL enzymes vol.107, 2017, https://doi.org/10.1016/j.freeradbiomed.2016.11.030
  4. Peroxisomes as Modulators of Cellular Protein Thiol Oxidation: A New Model System 2017, https://doi.org/10.1089/ars.2017.6997
  5. PRDX2 in Myocyte Hypertrophy and Survival is Mediated by TLR4 in Acute Infarcted Myocardium vol.7, pp.1, 2017, https://doi.org/10.1038/s41598-017-06718-7
  6. Expression of the Antioxidative Enzyme Peroxiredoxin 2 in Multiple Sclerosis Lesions in Relation to Inflammation vol.18, pp.4, 2017, https://doi.org/10.3390/ijms18040760
  7. Overview on Peroxiredoxin vol.39, pp.1, 2016, https://doi.org/10.14348/molcells.2016.2368
  8. Identification of MicroRNAs Involved in Growth Arrest and Apoptosis in Hydrogen Peroxide-Treated Human Hepatocellular Carcinoma Cell Line HepG2 vol.2016, 2016, https://doi.org/10.1155/2016/7530853
  9. Placental Proteomics Provides Insights into Pathophysiology of Pre-Eclampsia and Predicts Possible Markers in Plasma vol.16, pp.2, 2017, https://doi.org/10.1021/acs.jproteome.6b00955
  10. The active site architecture in peroxiredoxins: a case study on Mycobacterium tuberculosis AhpE vol.52, pp.67, 2016, https://doi.org/10.1039/C6CC02645A
  11. Mitochondrial peroxiredoxins are essential in regulating the relationship between Drosophila immunity and aging vol.1863, pp.1, 2017, https://doi.org/10.1016/j.bbadis.2016.10.017
  12. Control and dysregulation of redox signalling in the gastrointestinal tract pp.1759-5053, 2018, https://doi.org/10.1038/s41575-018-0079-5
  13. The Role of Peroxiredoxins in Various Diseases Caused by Oxidative Stress and the Prospects of Using Exogenous Peroxiredoxins vol.63, pp.4, 2018, https://doi.org/10.1134/S0006350918040164
  14. cytosolic tryparedoxin peroxidase in human natural infection vol.155, pp.3, 2018, https://doi.org/10.1111/imm.12979
  15. Detection of peroxiredoxin-like protein in Antarctic sea urchin (Sterechinus neumayeri) under heat stress and induced with pathogen-associated molecular pattern from Vibrio anguillarum vol.41, pp.10, 2018, https://doi.org/10.1007/s00300-018-2346-x
  16. The Multifaceted Impact of Peroxiredoxins on Aging and Disease vol.29, pp.13, 2018, https://doi.org/10.1089/ars.2017.7452
  17. Proteomics and Toxicity Analysis of Spinal-Cord Primary Cultures upon Hydrogen Sulfide Treatment vol.7, pp.7, 2018, https://doi.org/10.3390/antiox7070087
  18. Redox Signaling from and to Peroxisomes: Progress, Challenges, and Prospects pp.1557-7716, 2018, https://doi.org/10.1089/ars.2018.7515
  19. Severity of Systemic Inflammatory Response Syndrome Affects the Blood Levels of Circulating Inflammatory-Relevant MicroRNAs vol.8, pp.1664-3224, 2017, https://doi.org/10.3389/fimmu.2017.01977
  20. Identification of protein clusters predictive of tumor response in rectal cancer patients receiving neoadjuvant chemo-radiotherapy vol.8, pp.17, 2016, https://doi.org/10.18632/oncotarget.16053
  21. Emerging Therapeutic Targets in Oncologic Photodynamic Therapy vol.24, pp.44, 2016, https://doi.org/10.2174/1381612825666190122163832
  22. Dual function of peroxiredoxin I in lipopolysaccharide-induced osteoblast apoptosis via reactive oxygen species and the apoptosis signal-regulating kinase 1 signaling pathway vol.4, pp.None, 2018, https://doi.org/10.1038/s41420-018-0050-9
  23. 홍어 콜라겐 펩타이드의 산화적 스트레스 완화를 통한 항염증효과 vol.35, pp.4, 2016, https://doi.org/10.12925/jkocs.2018.35.4.1369
  24. Ethanolic leaf extract from Strophanthus gratus (Hook.) Franch. (Apocynaceae) exhibits anti-inflammatory and antioxidant activities vol.5, pp.1, 2016, https://doi.org/10.1080/23312025.2019.1710431
  25. Peroxisomal Hydrogen Peroxide Metabolism and Signaling in Health and Disease vol.20, pp.15, 2016, https://doi.org/10.3390/ijms20153673
  26. Characterization of extracellular redox enzyme concentrations in response to exercise in humans vol.127, pp.3, 2016, https://doi.org/10.1152/japplphysiol.00340.2019
  27. Catalysis of Peroxide Reduction by Fast Reacting Protein Thiols : Focus Review vol.119, pp.19, 2016, https://doi.org/10.1021/acs.chemrev.9b00371
  28. The overexpression of peroxiredoxin-4 affects the progression of idiopathic pulmonary fibrosis vol.19, pp.1, 2016, https://doi.org/10.1186/s12890-019-1032-2
  29. Peroxiredoxins and Immune Infiltrations in Colon Adenocarcinoma: Their Negative Correlations and Clinical Significances, an In Silico Analysis vol.11, pp.11, 2016, https://doi.org/10.7150/jca.38057
  30. A Novel Thioredoxin-Dependent Peroxiredoxin (TPx-Q) Plays an Important Role in Defense Against Oxidative Stress and Is a Possible Drug Target in Babesia microti vol.7, pp.None, 2016, https://doi.org/10.3389/fvets.2020.00076
  31. The C . elegans CHP1 homolog, pbo-1 , functions in innate immunity by regulating the pH of the intestinal lumen vol.16, pp.1, 2020, https://doi.org/10.1371/journal.ppat.1008134
  32. Prx2 (Peroxiredoxin 2) as a Cause of Hydrocephalus After Intraventricular Hemorrhage vol.51, pp.5, 2020, https://doi.org/10.1161/strokeaha.119.028672
  33. Ablation of Peroxiredoxin V Exacerbates Ischemia/Reperfusion-Induced Kidney Injury in Mice vol.9, pp.8, 2016, https://doi.org/10.3390/antiox9080769
  34. A novel peroxiredoxin from the antagonistic endophytic bacterium Enterobacter sp. V1 contributes to cotton resistance against Verticillium dahliae vol.454, pp.1, 2016, https://doi.org/10.1007/s11104-020-04661-7
  35. Protein signatures of seminal plasma from bulls with contrasting frozen-thawed sperm viability vol.10, pp.None, 2016, https://doi.org/10.1038/s41598-020-71015-9
  36. Global Proteomic Profiling of Piscirickettsia salmonis and Salmon Macrophage-Like Cells during Intracellular Infection vol.8, pp.12, 2020, https://doi.org/10.3390/microorganisms8121845
  37. A Complex Proteomic Response of the Parasitic Nematode Anisakis simplex s.s. to Escherichia coli Lipopolysaccharide vol.20, pp.None, 2016, https://doi.org/10.1016/j.mcpro.2021.100166
  38. Acute Running and Coronary Heart Disease Risk Markers in Male Cigarette Smokers and Nonsmokers: A Randomized Crossover Trial vol.53, pp.5, 2021, https://doi.org/10.1249/mss.0000000000002560
  39. Redox Enzymes of the Thioredoxin Family as Potential and Novel Markers in Pemphigus vol.2021, pp.None, 2016, https://doi.org/10.1155/2021/6672693
  40. Methylome Patterns of Cattle Adaptation to Heat Stress vol.12, pp.None, 2021, https://doi.org/10.3389/fgene.2021.633132
  41. Emerging Evidence Highlighting the Importance of Redox Dysregulation in the Pathogenesis of Amyotrophic Lateral Sclerosis (ALS) vol.14, pp.None, 2016, https://doi.org/10.3389/fncel.2020.581950
  42. Withania somnifera (L.) Dunal: Opportunity for Clinical Repurposing in COVID-19 Management vol.12, pp.None, 2016, https://doi.org/10.3389/fphar.2021.623795
  43. Multi–cell type gene coexpression network analysis reveals coordinated interferon response and cross–cell type correlations in systemic lupus erythematosus vol.31, pp.4, 2021, https://doi.org/10.1101/gr.265249.120
  44. Social modulation of ageing: mechanisms, ecology, evolution vol.376, pp.1823, 2021, https://doi.org/10.1098/rstb.2019.0738
  45. The cytosolic tryparedoxin peroxidase from Trypanosoma cruzi induces a pro‐inflammatory Th1 immune response in a peroxidatic cysteine‐dependent manner vol.163, pp.1, 2016, https://doi.org/10.1111/imm.13302
  46. Engineering Extracellular Vesicles Restore the Impaired Cellular Uptake and Attenuate Intervertebral Disc Degeneration vol.15, pp.9, 2021, https://doi.org/10.1021/acsnano.1c04514
  47. In vitro study of sodium butyrate on soyasaponin challenged intestinal epithelial cells of turbot (Scophthalmus maximus L.) refer to inflammation, apoptosis and antioxidant enzymes vol.2, pp.None, 2016, https://doi.org/10.1016/j.fsirep.2021.100031
  48. Proteome profiling of human placenta reveals developmental stage-dependent alterations in protein signature vol.18, pp.1, 2016, https://doi.org/10.1186/s12014-021-09324-y
  49. The molecular interplay of the establishment of an infection - gene expression of Diaphorina citri gut and Candidatus Liberibacter asiaticus vol.22, pp.1, 2016, https://doi.org/10.1186/s12864-021-07988-2
  50. A fingerprint of plasma proteome alteration after local tissue damage induced by Bothrops leucurus snake venom in mice vol.253, pp.None, 2016, https://doi.org/10.1016/j.jprot.2021.104464
  51. Peroxiredoxin 6 protects irradiated cells from oxidative stress and shapes their senescence-associated cytokine landscape vol.49, pp.None, 2016, https://doi.org/10.1016/j.redox.2021.102212