Molecules and Cells

  • 제39권1호
  • /
  • Pages.46-52
  • /
  • 2016
  • /
  • 1016-8478(pISSN)
  • /
  • 0219-1032(eISSN)
한국분자세포생물학회 (Korean Society for Molecular and Cellular Biology)
권호 표지
DOI QR코드

DOI QR Code

Utilizing Natural and Engineered Peroxiredoxins As Intracellular Peroxide Reporters

  • Laer, Koen Van (Division of Redox Regulation, DKFZ-ZMBH Alliance, German Cancer Research Center) ;
  • Dick, Tobias P. (Division of Redox Regulation, DKFZ-ZMBH Alliance, German Cancer Research Center)
  • 투고 : 2015.12.03
  • 심사 : 2015.12.06
  • 발행 : 2016.01.31
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

It is increasingly apparent that nature evolved peroxiredoxins not only as $H_2O_2$ scavengers but also as highly sensitive $H_2O_2$ sensors and signal transducers. Here we ask whether the $H_2O_2$ sensing role of Prx can be exploited to develop probes that allow to monitor intracellular $H_2O_2$ levels with unprecedented sensitivity. Indeed, simple gel shift assays visualizing the oxidation of endogenous 2-Cys peroxiredoxins have already been used to detect subtle changes in intracellular $H_2O_2$ concentration. The challenge however is to create a genetically encoded probe that offers real-time measurements of $H_2O_2$ levels in intact cells via the Prx oxidation state. We discuss potential design strategies for Prx-based probes based on either the redoxsensitive fluorophore roGFP or the conformation-sensitive fluorophore cpYFP. Furthermore, we outline the structural and chemical complexities which need to be addressed when using Prx as a sensing moiety for $H_2O_2$ probes. We suggest experimental strategies to investigate the influence of these complexities on probe behavior. In doing so, we hope to stimulate the development of Prx-based probes which may spearhead the further study of cellular $H_2O_2$ homeostasis and Prx signaling.

키워드

참고문헌

  1. Aslund, F., Zheng, M., Beckwith, J., and Storz, G. (1999). Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc. Natl. Acad. Sci. USA 96, 6161-6165. https://doi.org/10.1073/pnas.96.11.6161
  2. Barata, A.G., and Dick, T.P. (2013). In vivo imaging of H2O2 production in Drosophila. Methods Enzymol. 526, 61-82. https://doi.org/10.1016/B978-0-12-405883-5.00004-1
  3. Barranco-Medina, S., Lazaro, J.J., and Dietz, K.J. (2009). The oligomeric conformation of peroxiredoxins links redox state to function. FEBS Lett. 583, 1809-1816. https://doi.org/10.1016/j.febslet.2009.05.029
  4. Bilan, D., and Belousov, V. (2015). HyPer family probes: state of the art. Antioxid. Redox Signal. [Epub ahead of Print] doi:10.1089/ars.2015.6586.
  5. Cao, Z., Bhella, D., and Lindsay, J.G. (2007). Reconstitution of the mitochondrial PrxIII antioxidant defence pathway: general properties and factors affecting PrxIII activity and oligomeric state. J. Mol. Biol. 372, 1022-1033. https://doi.org/10.1016/j.jmb.2007.07.018
  6. Chae, H.Z., Oubrahim, H., Park, J.W., Rhee, S.G., and Chock, P.B. (2012). Protein glutathionylation in the regulation of peroxiredoxins:a family of thiol-specific peroxidases that function as antioxidants, molecular chaperones, and signal modulators. Antioxid. Redox Signal. 16, 506-523. https://doi.org/10.1089/ars.2011.4260
  7. Chang, T.S., Jeong, W., Choi, S.Y., Yu, S., Kang, S.W., and Rhee, S.G. (2002). Regulation of peroxiredoxin I activity by Cdc2-mediated phosphorylation. J. Biol. Chem. 277, 25370-25376. https://doi.org/10.1074/jbc.M110432200
  8. Cox, A.G., Pullar, J.M., Hughes, G., Ledgerwood, E.C., and Hampton, M.B. (2008). Oxidation of mitochondrial peroxiredoxin 3 during the initiation of receptor-mediated apoptosis. Free Rad. Biol. Med. 44, 1001-1009. https://doi.org/10.1016/j.freeradbiomed.2007.11.017
  9. Cox, A.G., Winterbourn, C.C., and Hampton, M.B. (2010). Measuring the redox state of cellular peroxiredoxins by immunoblotting. Methods Enzymol. 474, 51-66. https://doi.org/10.1016/S0076-6879(10)74004-0
  10. Delaunay, A., Pflieger, D., Barrault, M.B., Vinh, J. and Toledano, M.B. (2002). A thiol peroxidase is an H2O2 receptor and redoxtransducer in gene activation. Cell 111, 471-481. https://doi.org/10.1016/S0092-8674(02)01048-6
  11. Ermakova, Y.G., Bilan, D.S., Matlashov, M.E., Mishina, N.M., Markvicheva, K.N., Subach, O.M., Subach, F.V., Bogeski, I., Hoth, M., Enikolopov, G., et al. (2014). Red fluorescent genetically encoded indicator for intracellular hydrogen peroxide. Nat. Commun. 5, 5222. https://doi.org/10.1038/ncomms6222
  12. Ezerina, D., Morgan, B. and Dick, T.P. (2014) Imaging dynamic redox processes with genetically encoded probes. J. Mol. Cell. Cardiol. 73, 43-49. https://doi.org/10.1016/j.yjmcc.2013.12.023
  13. Hall, A., Nelson, K., Poole, L.B., and Karplus, P.A. (2011). Structurebased insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxid. Redox Signal. 15, 795-815. https://doi.org/10.1089/ars.2010.3624
  14. Hall, A., Sankaran, B., Poole, L.B., and Karplus, P.A. (2009). Structural changes common to catalysis in the Tpx peroxiredoxin subfamily. J. Mol. Biol. 393, 867-881. https://doi.org/10.1016/j.jmb.2009.08.040
  15. Jang, H.H., Kim, S.Y., Park, S.K., Jeon, H.S., Lee, Y.M., Jung, J.H., Lee, S.Y., Chae, H.B., Jung, Y.J., Lee, K.O., et al. (2006). Phosphorylation and concomitant structural changes in human 2-Cys peroxiredoxin isotype I differentially regulate its peroxidase and molecular chaperone functions. FEBS Lett. 580, 351-355. https://doi.org/10.1016/j.febslet.2005.12.030
  16. Konig, J., Galliardt, H., Jutte, P., Schaper, S., Dittmann, L., and Dietz, K.J. (2013). The conformational bases for the two functionalities of 2-Cysteine peroxiredoxins as peroxidase and chaperone. J. Exp. Bot. 64, 3483-3497. https://doi.org/10.1093/jxb/ert184
  17. Koo, K.H., Lee, S., Jeong, S.Y., Kim, E.T., Kim, H.J., Kim, K., Song, K., and Chae, H.Z. (2002). Regulation of thioredoxin peroxidase activity by C-terminal truncation. Arch. Biochem. Biophys. 397, 312-318. https://doi.org/10.1006/abbi.2001.2700
  18. Kumar, V., Kitaeff, N., Hampton, M.B., Cannell, M.B., and Winterbourn, C.C. (2009). Reversible oxidation of mitochondrial peroxiredoxin 3 in mouse heart subjected to ischemia and reperfusion. FEBS Lett. 583, 997-1000. https://doi.org/10.1016/j.febslet.2009.02.018
  19. Moon, J.C., Kim, G.M., Kim, E.K., Lee, H.N., Ha, B., Lee, S.Y., and Jang, H.H. (2013). Reversal of 2-Cys peroxiredoxin oligomerization by sulfiredoxin. Biochem. Biophys. Res. Commun. 432, 291-295. https://doi.org/10.1016/j.bbrc.2013.01.114
  20. Muthuramalingam, M., Seidel, T., Laxa, M., Nunes de Miranda, S.M., Gartner, F., Stroher, E., Kandlbinder, A., and Dietz, K.J. (2009). Multiple redox and non-redox interactions define 2-Cys peroxiredoxin as a regulatory hub in the chloroplast. Mol. Plant 2, 1273-1288. https://doi.org/10.1093/mp/ssp089
  21. Nelson, K.J., Parsonage, D., Karplus, P.A., and Poole, L.B. (2013). Evaluating peroxiredoxin sensitivity toward inactivation by peroxide substrates. Method Enzymol. 527, 21-40. https://doi.org/10.1016/B978-0-12-405882-8.00002-7
  22. Noichri, Y., Palais, G., Ruby, V., D'Autreaux, B., Delaunay-Moisan, A., Nystrom, T., Molin, M., and Toledano, M.B. (2015). In vivo parameters influencing 2-Cys Prx oligomerization: The role of enzyme sulfinylation. Redox Biol. 6, 326-333. https://doi.org/10.1016/j.redox.2015.08.011
  23. Parsonage, D., Youngblood, D.S., Sarma, G.N., Wood, Z.A., Karplus, P.A., and Poole, L.B. (2005). Analysis of the link between enzymatic activity and oligomeric state in AhpC, a bacterial peroxiredoxin. Biochemistry 44, 10583-10592. https://doi.org/10.1021/bi050448i
  24. Parsonage, D., Karplus, P.A., and Poole, L.B. (2008). Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin. Proc. Natl. Acad. Sci. USA 105, 8209-8214. https://doi.org/10.1073/pnas.0708308105
  25. Perkins, A., Poole, L.B., and Karplus, P.A. (2014). Tuning of peroxiredoxin catalysis for various physiological roles. Biochemistry 53, 7693-7705. https://doi.org/10.1021/bi5013222
  26. 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
  27. Poynton, R.A., and Hampton, M.B. (2014). Peroxiredoxins as biomarkers of oxidative stress. Biochimica Biophys. Acta 1840, 906-912. https://doi.org/10.1016/j.bbagen.2013.08.001
  28. Qu, D., Rashidian, J., Mount, M.P., Aleyasin, H., Parsanejad, M., Lira, A., Haque, E., Zhang, Y., Callaghan, S., Daigle, M., et al. (2007). Role of Cdk5-mediated phosphorylation of Prx2 in MPTP toxicity and Parkinson's disease. Neuron 55, 37-52. https://doi.org/10.1016/j.neuron.2007.05.033
  29. Randall, L.M., Manta, B., Hugo, M., Gil, M., Batthyany, C., Trujillo, M., Poole, L.B., and Denicola, A. (2014). Nitration transforms a sensitive peroxiredoxin 2 into a more active and robust peroxidase. J. Biol. Chem. 289, 15536-15543. https://doi.org/10.1074/jbc.M113.539213
  30. Rhee, S.G., and Woo, H.A. (2011). Multiple functions of peroxiredoxins:peroxidases, sensors and regulators of the intracellular messenger H(2)O(2), and protein chaperones. Antioxid. Redox Signal. 15, 781-794. https://doi.org/10.1089/ars.2010.3393
  31. Rhee, S.G., Woo, H.A., Kil, I.S., and Bae, S.H. (2012). Peroxiredoxin Functions as a Peroxidase and a Regulator and Sensor of Local Peroxides. J. Biol. Chem. 287, 4403-4410. https://doi.org/10.1074/jbc.R111.283432
  32. Sayed, A.A., and Williams, D.L. (2004). Biochemical characterization of 2-Cys peroxiredoxins from Schistosoma mansoni. J. Biol. Chem. 279, 26159-26166. https://doi.org/10.1074/jbc.M401748200
  33. Schwarzlander, M., Dick, T.P., Meyer, A.J., and Morgan, B. (2015). Dissecting redox biology using fluorescent protein sensors. Antioxid. Redox Signal. [Epub ahead of print]. dio:10.1089/ars.2015.6266
  34. Seidel, T., Seefeldt, B., Sauer, M., and Dietz, K.J. (2010). In vivo analysis of the 2-Cys peroxiredoxin oligomeric state by two-step FRET. J. Biotechnol. 149, 272-279. https://doi.org/10.1016/j.jbiotec.2010.06.016
  35. Seo, J.H., Lim, J.C., Lee, D.Y., Kim, K.S., Piszczek, G., Nam, H.W., Kim, Y.S., Ahn, T., Yun, C.H., Kim, K., et al. (2009). Novel protective mechanism against irreversible hyperoxidation of peroxiredoxin: Nalpha-terminal acetylation of human peroxiredoxin II. J. Biol. Chem. 284, 13455-13465. https://doi.org/10.1074/jbc.M900641200
  36. Sobotta, M.C., Barata, A.G., Schmidt, U., Mueller, S., Millonig, G., and Dick, T.P. (2013). Exposing cells to H2O2: a quantitative comparison between continuous low-dose and one-time highdose treatments. Free Rad. Biol. Med. 60, 325-335. https://doi.org/10.1016/j.freeradbiomed.2013.02.017
  37. 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 H2O2 signaling. Nat. Chem. Biol. 11, 64-70. https://doi.org/10.1038/nchembio.1695
  38. Tarrago, L., Peterfi, Z., Lee, B.C., Michel, T., and Gladyshev, V.N. (2015). Monitoring methionine sulfoxide with stereospecific mechanism-based fluorescent sensors. Nat. Chem. Biol. 11, 332-338. https://doi.org/10.1038/nchembio.1787
  39. Teixeira, F., Castro, H., Cruz, T., Tse, E., Koldewey, P., Southworth, D.R., Tomas, A.M., and Jakob, U. (2015). Mitochondrial peroxiredoxin functions as crucial chaperone reservoir in Leishmania infantum. Proc. Natl. Acad. Sci. USA 112, E616-624. https://doi.org/10.1073/pnas.1419682112
  40. Trujillo, M., Clippe, A., Manta, B., Ferrer-Sueta, G., Smeets, A., Declercq, J.P., Knoops, B., and Radi, R. (2007). Pre-steady state kinetic characterization of human peroxiredoxin 5: taking advantage of Trp84 fluorescence increase upon oxidation. Arch. Biochem. Biophys. 467, 95-106. https://doi.org/10.1016/j.abb.2007.08.008
  41. Wang, X., Wang, L.K., Wang, X., Sun, F., and Wang, C.C. (2012). Structural insights into the peroxidase activity and inactivation of human peroxiredoxin 4. Biochem. J. 441, 113-118. https://doi.org/10.1042/BJ20110380
  42. Winterbourn, C.C. (2013). The biological chemistry of hydrogen peroxide. Methods Enzymol. 528, 3-25. https://doi.org/10.1016/B978-0-12-405881-1.00001-X
  43. Wood, Z.A., Poole, L.B., and Karplus, P.A. (2003). Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300, 650-653. https://doi.org/10.1126/science.1080405
  44. Zhao, Y., Araki, S., Wu, J., Teramoto, T., Chang, Y.F., Nakano, M., Abdelfattah, A.S., Fujiwara, M., Ishihara, T., Nagai, T., et al. (2011). An expanded palette of genetically encoded Ca(2)(+) indicators. Science 333, 1888-1891. https://doi.org/10.1126/science.1208592
  45. Zykova, T.A., Zhu, F., Vakorina, T.I., Zhang, J., Higgins, L.A., Urusova, D.V., Bode, A.M., and Dong, Z. (2010). T-LAK cell-originated protein kinase (TOPK) phosphorylation of Prx1 at Ser-32 prevents UVB-induced apoptosis in RPMI7951 melanoma cells through the regulation of Prx1 peroxidase activity. J. Biol. Chem. 285, 29138-29146. https://doi.org/10.1074/jbc.M110.135905

피인용 문헌

  1. The Role of Peroxiredoxins in the Transduction of H2O2 Signals 2018, https://doi.org/10.1089/ars.2017.7167
  2. Mitochondrial ROS control of cancer 2017, https://doi.org/10.1016/j.semcancer.2017.04.005
  3. Overview on Peroxiredoxin vol.39, pp.1, 2016, https://doi.org/10.14348/molcells.2016.2368
  4. Thiol-based copper handling by the copper chaperone Atox1 vol.69, pp.4, 2017, https://doi.org/10.1002/iub.1620
  5. Monitoring the action of redox-directed cancer therapeutics using a human peroxiredoxin-2-based probe vol.9, pp.1, 2018, https://doi.org/10.1038/s41467-018-05557-y
  6. Strategies to detect mitochondrial oxidants vol.21, pp.None, 2016, https://doi.org/10.1016/j.redox.2018.101065
  7. Enzymatic Antioxidant Signatures in Hyperthermophilic Archaea vol.9, pp.8, 2020, https://doi.org/10.3390/antiox9080703
  8. 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
  9. Measuring Reactive Sulfur Species and Thiol Oxidation States: Challenges and Cautions in Relation to Alkylation-Based Protocols vol.33, pp.16, 2020, https://doi.org/10.1089/ars.2020.8077