Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

A Cytosolic Thioredoxin Acts as a Molecular Chaperone for Peroxisome Matrix Proteins as Well as Antioxidant in Peroxisome

  • Du, Hui (Department of Biological Science, Sookmyung Women's University) ;
  • Kim, Sunghan (Department of Plant Science, Seoul National University) ;
  • Hur, Yoon-Sun (Department of Biological Science, Sookmyung Women's University) ;
  • Lee, Myung-Sok (Department of Biological Science, Sookmyung Women's University) ;
  • Lee, Suk-Ha (Department of Plant Science, Seoul National University) ;
  • Cheon, Choong-Ill (Department of Biological Science, Sookmyung Women's University)
  • Received : 2014.09.18
  • Accepted : 2014.12.18
  • Published : 2015.02.28
Download PDF
⟨ Previous Next ⟩

Abstract

Thioredoxin (TRX) is a disulfide reductase present ubiquitously in all taxa and plays an important role as a regulator of cellular redox state. Recently, a redox-independent, chaperone function has also been reported for some thioredoxins. We previously identified nodulin-35, the subunit of soybean uricase, as an interacting target of a cytosolic soybean thioredoxin, GmTRX. Here we report the further characterization of the interaction, which turns out to be independent of the disulfide reductase function and results in the co-localization of GmTRX and nodulin-35 in peroxisomes, suggesting a possible function of GmTRX in peroxisomes. In addition, the chaperone function of GmTRX was demonstrated in in vitro molecular chaperone activity assays including the thermal denaturation assay and malate dehydrogenase aggregation assay. Our results demonstrate that the target of GmTRX is not only confined to the nodulin-35, but many other peroxisomal proteins, including catalase (AtCAT), transthyretin-like protein 1 (AtTTL1), and acyl-coenzyme A oxidase 4 (AtACX4), also interact with the GmTRX. Together with an increased uricase activity of nodulin-35 and reduced ROS accumulation observed in the presence of GmTRX in our results, especially under heat shock and oxidative stress conditions, it appears that GmTRX represents a novel thioredoxin that is co-localized to the peroxisomes, possibly providing functional integrity to peroxisomal proteins.

Keywords

References

  1. Arent, S., Christensen, C.E., Pye, V.E., Norgaard, A., and Henriksen, A. (2010). The multifunctional protein in peroxisomal betaoxidation: structure and substrate specificity of the Arabidopsis thaliana protein MFP2. J. Biol. Chem. 285, 24066-24077. https://doi.org/10.1074/jbc.M110.106005
  2. Balmer, Y., Vensel, W.H., Tanaka, C.K., Hurkman, W.J., Gelhaye, E., Rouhier, N., Jacquot, J.P., Manieri, W., Schurmann, P., Droux, M., et al. (2004). Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc. Natl. Acad. Sci. USA 101, 2642-2647. https://doi.org/10.1073/pnas.0308583101
  3. Bartsch, S., Monnet, J., Selbach, K., Quigley, F., Gray, J., von Wettstein, D., Reinbothe, S., and Reinbothe, C. (2008). Three thioredoxin targets in the inner envelope membrane of chloroplasts function in protein import and chlorophyll metabolism. Proc. Natl. Acad. Sci. USA 105, 4933-4938. https://doi.org/10.1073/pnas.0800378105
  4. Borges, A.A., Borges-Perez, A., and Fernandez-Falcon M. (2003). Effect of menadione sodium bisulfite, an inducer of plant defenses, on the dynamic of banana phytoalexin accumulation during pathogenesis. J. Agric. Food Chem. 27, 5326-5328.
  5. Collet, J.F., and Messens, J. (2010). Structure, function, and mechanism of thioredoxin proteins. Antioxid. Redox Signal. 13, 1205-1216. https://doi.org/10.1089/ars.2010.3114
  6. Courteille, A., Vesa, S., Sanz-Barrio, R., Cazale, A.C., Becuwe- Linka, N., Farran, I., Havaux, M., Rey, P., and Rumeau, D. (2013). Thioredoxin m4 controls photosynthetic alternative electron pathways in Arabidopsis. Plant Physiol. 161, 508-520. https://doi.org/10.1104/pp.112.207019
  7. Couturier, J., Chibani, K., Jacquot, J.P., and Rouhier, N. (2013). Cysteine-based redox regulation and signaling in plants. Front. Plant Sci. 4, 105.
  8. Du, H., Kim, S., Nam, K.H., Lee, M.S., Son, O., Lee, S.H., and Cheon, C.I. (2010). Identification of uricase as a potential target of plant thioredoxin: Implication in the regulation of nodule development. Biochem. Biophys. Res. Commun. 397, 22-26. https://doi.org/10.1016/j.bbrc.2010.05.040
  9. Gelhaye, E., Rouhier, N., Gerard, J., Jolivet, Y., Gualberto, J., Navrot, N., Ohlsson, P.I., Wingsle, G., Hirasawa, M., Knaff, D.B., et al. (2004). A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc. Natl. Acad. Sci. USA 101, 14545-14550. https://doi.org/10.1073/pnas.0405282101
  10. Gelhaye, E., Rouhier, N., Navrot, N., and Jacquot, J.P. (2005). The plant thioredoxin system. Cell Mol. Life Sci. 62, 24-35. https://doi.org/10.1007/s00018-004-4296-4
  11. Gomes, A., Fernandes, E., and Lima, J.L. (2005). Fluorescence probes used for detection of reactive oxygen species. J. Biochem. Biophys. Methods 65, 45-80. https://doi.org/10.1016/j.jbbm.2005.10.003
  12. Guan, Q., Lu, X., Zeng, H., Zhang, Y., and Zhu, J. (2013). Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J. 74, 840-851. https://doi.org/10.1111/tpj.12169
  13. Hu, J., Baker, A., Bartel, B., Linka, N., Mullen, R.T., Reumann, S., and Zolman, B.K. (2012). Plant peroxisomes: biogenesis and function. Plant Cell 24, 2279-2303. https://doi.org/10.1105/tpc.112.096586
  14. Kern, R., Malki, A., Holmgren, A., and Richarme, G. (2003). Chaperone properties of Escherichia coli thioredoxin and thioredoxin reductase. Biochem. J. 371, 965-972. https://doi.org/10.1042/bj20030093
  15. Kthiri, F., Le, H.T., Tagourti, J., Kern, R., Malki, A., Caldas, T., Abdallah, J., Landoulsi, A., and Richarme, G. (2008). The thioredoxin homolog YbbN functions as a chaperone rather than as an oxidoreductase. Biochem. Biophys. Res. Commun. 374, 668-672. https://doi.org/10.1016/j.bbrc.2008.07.080
  16. Kumar, J.K., Tabor, S., and Richardson, C.C. (2004). Proteomic analysis of thioredoxin-targeted proteins in Escherichia coli. Proc. Natl. Acad. Sci. USA. 101, 3759-3764. https://doi.org/10.1073/pnas.0308701101
  17. Lamberto, I., Percudani, R., Gatti, R., Folli, C., and Petrucco, S. (2010). Conserved alternative splicing of Arabidopsis transthyretin-like determines protein localization and S-allantoin synthesis in peroxisomes. Plant Cell 22, 1564-1574. https://doi.org/10.1105/tpc.109.070102
  18. Lee, M.Y., Shin, K.H., Kim, Y.K., Suh, J.Y., Gu, Y.Y., Kim, M.R., Hur, Y.S., Son, O., Kim, J.S., Song, E., et al. (2005). Induction of thioredoxin is required for nodule development to reduce reactive oxygen species levels in soybean roots. Plant Physiol. 139, 1881-1889. https://doi.org/10.1104/pp.105.067884
  19. Lee, J.R., Lee, S.S., Jang, H.H., Lee, Y.M., Park, J.H., Park, S.C., Moon, J.C., Park, S.K., Kim, S.Y., Lee, S.Y., et al. (2009). Heatshock dependent oligomeric status alters the function of a plantspecific thioredoxin-like protein, AtTDX. Proc. Natl. Acad. Sci. USA 106, 5978-5983. https://doi.org/10.1073/pnas.0811231106
  20. Lemaire, S.D., Michelet, L., Zaffagnini, M., Massot, V., and Issakidis- Bourguet, E. (2007). Thioredoxins in chloroplasts. Curr. Genet. 51, 343-365. https://doi.org/10.1007/s00294-007-0128-z
  21. Meng, L., Wong, J.H., Feldman, L.J., Lemaux P.G., and Buchanan, B.B. (2010). A membrane-associated thioredoxin required for plant growth moves from cell to cell, suggestive of a role in intercellular communication. Proc. Natl. Acad. Sci. USA 107, 3900-3905. https://doi.org/10.1073/pnas.0913759107
  22. Meyer, Y., Reichheld, J.P., and Vignols, F. (2005). Thioredoxins in Arabidopsis and other plants. Photosynth. Res. 86, 419-433. https://doi.org/10.1007/s11120-005-5220-y
  23. Neuspiel, M., Schauss, A.C., Braschi, E., Zunino, R., Rippstein, P., Rachubinski, R.A., Andrade-Navarro, M.A., and McBride, H.M. (2008). Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr. Biol. 18, 102-108. https://doi.org/10.1016/j.cub.2007.12.038
  24. Nuruzzaman, M., Sharoni, A.M., Satoh, K., Al-Shammari, T., Shimizu, T., Sasaya, T., Omura, T., and Kikuchi, S. (2012). The thioredoxin gene family in rice: genome-wide identification and expression profiling under different biotic and abiotic treatments. Biochem. Biophys. Res. Commun. 423, 417-423. https://doi.org/10.1016/j.bbrc.2012.05.142
  25. Park, S.K., Jung, Y.J., Lee, J.R., Lee, Y.M., Jang, H.H., Lee, S.S., Park, J.H., Kim, S.Y., Moon, J.C., Lee, S.Y., et al. (2009). Heat-shock and redox-dependent functional switching of an h-type Arabidopsis thioredoxin from a disulfide reductase to a molecular chaperone. Plant Physiol. 150, 552-561. https://doi.org/10.1104/pp.109.135426
  26. Santhoshkumar, P., and Sharma, K.K. (2001). Analysis of alphacrystallin chaperone function using restriction enzymes and citrate synthase. Mol. Vis. 7, 172-177.
  27. Sanz-Barrio, R., Fernandez-San Millan, A., Carballeda, J., Corral- Martinez, P., Segui-Simarro, J.M., and Farran, I. (2012). Chaperone- like properties of tobacco plastid thioredoxins f and m. J. Exp. Bot. 63, 365-379. https://doi.org/10.1093/jxb/err282
  28. Scranton, M.A., Yee, A., Park, S.Y., and Walling, L.L. (2012). Plant leucine aminopeptidases moonlight as molecular chaperones to alleviate stress-induced damage. J. Biol. Chem. 287, 18408-18417. https://doi.org/10.1074/jbc.M111.309500
  29. Serrato, A.J., Crespo, J.L., Florencio, F.J., and Cejudo, F.J. (2001). Characterization of two thioredoxins h with predominant localization in the nucleus of aleurone and scutellum cells of germinating wheat seeds. Plant Mol. Biol. 46, 361-371. https://doi.org/10.1023/A:1010697331184
  30. Suzuki, H., and Verma, D.P. (1991). Soybean Nodule-Specific Uricase (Nodulin-35) Is Expressed and Assembled into a Functional Tetrameric Holoenzyme in Escherichia coli. Plant Physiol. 95, 384-389. https://doi.org/10.1104/pp.95.2.384
  31. Vacca, R.A., de Pinto, M.C., Valenti, D., Passarella, S., Marra, E, and De Gara, L. (2004). Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shockinduced programmed cell death in tobacco Bright-Yellow 2 cells. Plant Physiol. 134, 1100-1112. https://doi.org/10.1104/pp.103.035956
  32. Yamazaki, D., Motohashi, K., Kasama, T., Hara, Y., and Hisabori, T. (2005). Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana. Plant Cell Physiol. 45, 18-27.
  33. Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572. https://doi.org/10.1038/nprot.2007.199
  34. Zhang, L., Li, Y., Xing, D., and Gao, C. (2009). Characterization of mitochondrial dynamics and subcellular localization of ROS reveal that HsfA2 alleviates oxidative damage caused by heat stress in Arabidopsis. J. Exp. Bot. 60, 2073-2091. https://doi.org/10.1093/jxb/erp078
  35. Zhang, C.J., Zhao, B.C., Ge, W.N., Zhang, Y.F., Song, Y., Sun, D.Y., and Guo, Y. (2011). An apoplastic h-type thioredoxin is involved in the stress response through regulation of the apoplastic reactive oxygen species in rice. Plant Physiol. 157, 1884-1899. https://doi.org/10.1104/pp.111.182808

Cited by

  1. Identification of the Raptor-binding motif on Arabidopsis S6 kinase and its use as a TOR signaling suppressor vol.472, pp.1, 2016, https://doi.org/10.1016/j.bbrc.2016.02.068
  2. Proteome analysis reveals an energy-dependent central process for Populus × canadensis seed germination vol.213, 2017, https://doi.org/10.1016/j.jplph.2017.03.008
  3. Identification of nucleosome assembly protein 1 (NAP1) as an interacting partner of plant ribosomal protein S6 (RPS6) and a positive regulator of rDNA transcription vol.465, pp.2, 2015, https://doi.org/10.1016/j.bbrc.2015.07.150
  4. Molecular and Functional Characterization of a Rice Thioredoxin m Isoform and Its Interaction Proteins vol.23, pp.3, 2018, https://doi.org/10.1007/s12257-018-0133-8
  5. vol.203, pp.1, 2016, https://doi.org/10.1534/genetics.115.185272
  6. Pexophagy: Molecular Mechanisms and Implications for Health and Diseases vol.41, pp.1, 2015, https://doi.org/10.14348/molcells.2018.2245
  7. 인체 간암세포에서 비기환(肥氣丸), 대칠기탕(大七氣湯) 및 목향빈랑환(木香檳榔丸) 열수 추출물의 항암 활성 비교 vol.28, pp.1, 2015, https://doi.org/10.14374/hfs.2020.28.1.15
  8. Citronellal perception and transmission by Anopheles gambiae s.s. (Diptera: Culicidae) females vol.10, pp.1, 2015, https://doi.org/10.1038/s41598-020-75782-3
  9. Proteomic Analysis of Fusarium oxysporum-Induced Mechanism in Grafted Watermelon Seedlings vol.12, pp.None, 2021, https://doi.org/10.3389/fpls.2021.632758
  10. A small heat shock protein, GmHSP17.9, from nodule confers symbiotic nitrogen fixation and seed yield in soybean vol.20, pp.1, 2015, https://doi.org/10.1111/pbi.13698