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Multiple Roles of Peroxiredoxins in Inflammation
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  • Journal title : Molecules and Cells
  • Volume 39, Issue 1,  2016, pp.60-64
  • Publisher : Korea Society for Molecular and Cellular Biology
  • DOI : 10.14348/molcells.2016.2341
 Title & Authors
Multiple Roles of Peroxiredoxins in Inflammation
Knoops, Bernard; Argyropoulou, Vasiliki; Becker, Sarah; Ferte, Laura; Kuznetsova, Oksana;
  PDF(new window)
 Abstract
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.
 Keywords
inflammation;innate immunity;peroxiredoxins;reactive oxygen species;reactive nitrogen species;redox signaling;
 Language
English
 Cited by
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 References
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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

18.
Gretes, M.C., Poole, L.B., and Karplus, P.A. (2012). Peroxiredoxins in parasites. Antioxid. Redox Signal. 17, 608-633. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

30.
Knoops, B., Loumaye, E., and Van Der Eecken, V. (2007). Evolution of peroxiredoxins. Subcell. Biochem. 44, 27-40. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

50.
Royet, J., Reichhart, J.M., and Hoffmann, J.A. (2005). Sensing and signaling during infection in Drosophila. Curr. Opin. Immunol. 17, 11-17. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

55.
Sies, H. (2014). Role of Metabolic $H_2O_2$ Generation: redox signaling and oxidative stress. J. Biol. Chem. 289, 8735-8741. crossref(new window)

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.

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)