Skip to main content
SpringerLink
Log in

Xenopus laevis peroxiredoxins: Gene expression during development and characterization of the enzymes

  • Molecular Cell Biology
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

Reactive oxygen species (ROS) are produced via catabolic and anabolic processes during normal embryonic development, and ROS content in the cell is maintained at a certain level. Peroxiredoxins are a family of selenium-independent peroxidases and play a key role in maintaining redox homeostasis of the cell. In addition to regulating the ROS level, peroxiredoxins are involved in intracellular and intercellular signaling, cell differentiation, and tissue development. The time course of peroxiredoxin gene (prx1–6) expression was studied in Xenopus laevis during early ontogeny (Nieuwkoop and Faber stages 10–63). The highest expression level was observed for prx1 at these developmental stages. The prx1, prx3, and prx4 expression level changed most dramatically in response to oxidative stress artificially induced in X. laevis embryos. In X. laevis adults, prx1–6 were all intensely expressed in all organs examined, the prx1 expression level being the highest. The X. laevis prx1–6 genes were cloned and expressed in Escherichia coli, and physico-chemical characteristics were compared for the recombinant enzymes. The highest peroxidase activity and thermal stability were observed for Prx1 and Prx2. It was assumed that Prx1 plays a leading role in X. laevis early development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ROS:

reactive oxygen species

FR:

free radical

Prx:

peroxyredoxin

References

  1. Melekhova, O.P. 2010. Svobodnoradikal’nye protsessy v epigenomnoi regulyatsii razvitiya (Free Radial Processes in Epigenomic Regulation of Deelopment), Moscow: Nauka.

    Google Scholar 

  2. Saran M., Bors W. 1989. Oxygen radicals acting as chemical messengers: A hypothesis. Free Radic. Res. Commun. 7, 213–220.

    Article  CAS  PubMed  Google Scholar 

  3. Thomas M., Jain S., Kumar G.P., Laloraya M. 1997. A programmed oxyradical burst causes hatching of mouse blastocysts. J. Cell Sci. 110, 1597–1602

    CAS  PubMed  Google Scholar 

  4. Duran Reyes G., Gomez Melendez M.R., Hicks Gomez J.J. 1998. Importance of free radicals during the reproduction cycle. Ginecol. Obstet. Mex. 66, 371–376.

    CAS  PubMed  Google Scholar 

  5. Wallace R.A., Selman K. 1990. Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians. J. Electron Microsc. Tech. 16, 175–201.

    Article  CAS  PubMed  Google Scholar 

  6. Fantel A.G., Person R.E. 2002. Involvement of mitochondria and other free radicalsources in normal and abnormal fetal development. Ann. NY Acad. Sci. 959, 424–433.

    Article  CAS  PubMed  Google Scholar 

  7. Johnson M.H., Nasr-Esfahani M.H. 1994. Radical solutions and cultural problems: Could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? Bioessays. 16, 31–38.

    Article  CAS  PubMed  Google Scholar 

  8. Dennery P.A. 2010. Oxidative stress in development: Nature or nurture? Free Radic. Biol. Med. 49, 1147–1151.

    CAS  Google Scholar 

  9. Menon J., Rozman R. 2007. Oxidative stress, tissue remodeling and regression during amphibian metamorphosis. Comp. Biochem. Physiol. Toxicol. Pharmacol. 145, 625–631.

    Article  Google Scholar 

  10. Gagioti S., Colepicolo P., Bevilacqua E. 1995. Postimplantation mouse embryos have the capability to generate and release reactive oxygen species. Reprod. Fertil. Dev. 7, 1111–1116.

    Article  CAS  PubMed  Google Scholar 

  11. Salas-Vidal E., Lomeli H., Castro-Obregon S., Cuervo R., Escalante-Alcalde D., Covarrubias L. 1998. Reactive oxygen species participate in the control of mouse embryonic cell death. Exp. Cell. Res. 238, 136–147.

    Article  CAS  PubMed  Google Scholar 

  12. Johnson J., Manzo W., Gardner E., Menon J. 2013. Reactive oxygen species and anti-oxidant defenses in tail of tadpoles, Xenopus laevis. Comp. Biochem. Physiol. Toxicol. Pharmacol. 158, 101–108.

    Article  CAS  Google Scholar 

  13. Dennery P. A. 2004. Role of redox in fetal development and neonatal diseases. Antioxid. Redox Signaling. 6, 147–153.

    Article  CAS  Google Scholar 

  14. Hernandez-Garcia D., Wood C.D., Castro-Obregon S., Covarrubias L. 2010. Reactive oxygen species: A radical role in development? Free Radic. Biol. Med. 49, 130–143.

    Article  CAS  PubMed  Google Scholar 

  15. Cooper C.A., Walsh L.A., Damjanovski S. 2007. Peroxisome biogenesis occurs in late dorsal-anterior structures in the development of Xenopus laevis. Dev. Dyn. 236, 3554–3561.

    Article  CAS  PubMed  Google Scholar 

  16. Ciolek E., Vamecq J., Van Hoof F., Dauca M., Bautz A. 1989. Developmental patterns of peroxisomal enzymes in amphibian liver during spontaneous and triiodothyronine-induced metamorphosis. Comp. Biochem. Physiol. B. 93, 477–484.

    Article  CAS  PubMed  Google Scholar 

  17. Rizzo A.M., Adorni L., Montorfano G., Rossi F., Berra B. 2007. Antioxidant metabolism of Xenopus laevis embryos during the first days of development. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 146, 94–100.

    Article  Google Scholar 

  18. Flohe L., Harris J.R. 2007. Peroxiredoxin systems. Subcell. Biochem. 44, 1–25.

    Article  PubMed  Google Scholar 

  19. Sharapov M.G., Ravin V.K., Novoselov V.I. Peroxiredoxins as multifunctional enzymes. Mol. Biol. (Moscow). 48 (4), 520–545.

  20. Neumann C.A., Krause D.S., Carman C.V., Das S., Dubey D.P., Abraham J.L., Bronson R.T., Fujiwara Y., Orkin S.H., Van Etten R.A. 2003. Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature. 424, 561–565.

    Article  CAS  PubMed  Google Scholar 

  21. Lee T.H., Kim S.U., Yu S.L., Kim S.H., Park S., Moon H.B., Dho S.H., Kwon K.S., Kwon H.J., Han Y.H., Jeong S., Kang S.W., Shin H.S., Lee K.K., Rhee S.G., Yu D.Y. 2003. Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice. Blood. 101, 5033–5038.

    Article  CAS  PubMed  Google Scholar 

  22. Wonsey D.R., Zeller K.I., Dang C.V. 2002. The c-Myc target gene PRDX3 is required for mitochondrial homeostasis and neoplastic transformation. Proc. Natl. Acad. Sci. U. S. A. 99, 6649–6654.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Iuchi Y., Okada F., Tsunoda S., Kibe N., Shirasawa N., Ikawa M., Okabe M., Ikeda Y., Fujii J. 2009. Peroxiredoxin 4 knockout results in elevated spermatogenic cell death via oxidative stress. Biochem. J. 419, 149–158.

    Article  CAS  PubMed  Google Scholar 

  24. Wang X., Phelan S.A., Forsman-Semb K., Taylor E.F., Petros C., Brown A., Lerner C.P., Paigen B. 2003. Mice with targeted mutation of peroxiredoxin 6 develop normally but are susceptible to oxidative stress. J. Biol. Chem. 278, 25179–25190.

    Article  CAS  PubMed  Google Scholar 

  25. Nieuwkoop P.D., Faber J. 1956. Normal Table of Xenopus laevis (Daudin). A Systematic and Choronological Survey of the Development from The Fertilized Egg Till the End of Metamorphosis. Amsterdam: North Holland.

    Google Scholar 

  26. Livak K.J., Schmittgen T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) method. Methods. 25, 402–408.

    Article  CAS  PubMed  Google Scholar 

  27. Schmittgen T.D., Livak K.J. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108.

    Article  CAS  PubMed  Google Scholar 

  28. Kang S.W., Baines I.C., Rhee S.G. 1998. Characterization of a mammalian peroxiredoxin that contains one conserved cystein. J. Biol. Chem. 273, 6303–6311.

    Article  CAS  PubMed  Google Scholar 

  29. Sharapov M.G., Novoselov V.I., Ravin V.K. 2009. The cloning, expression, and comparative analysis of peroxiredoxin 6 from various sources. Mol. Biol. (Moscow). 43 (3), 465–471.

    Article  CAS  Google Scholar 

  30. Sharapov M.G., Ravin V.K. 2009. Peroxiredoxin 6 from the clawed frog Xenopus laevis: cDNA cloning, enzyme characterization, and gene expression during development. Biochemistry (Moscow). 74 (8), 898–902.

    CAS  PubMed  Google Scholar 

  31. Sharapov M.G., Novoselov V.I., Fesenko E.E., Ravin V.K. 2011. Two isoforms of peroxiredoxin 6 of Xenopus laevis. Mol. Biol. (Moscow). 46 (6), 933–940.

    Article  Google Scholar 

  32. Shafer M.E., Willson J.A., Damjanovski S. 2011. Expression analysis of the peroxiredoxin gene family during early development in Xenopus laevis. Gene Expr. Patterns. 11, 511–516.

    Article  CAS  PubMed  Google Scholar 

  33. Sindelka R., Ferjentsik Z., Jonak J. 2006. Developmental expression profiles of Xenopus laevis reference genes. Dev. Dyn. 235, 754–758.

    Article  CAS  PubMed  Google Scholar 

  34. Jang H.H., Lee K.O., Chi Y.H., Jung B.G., Park S.K., Park J.H., Lee J.R., Lee S.S., Moon J.C., Yun J.W., Choi Y.O., Kim W.Y., Kang J.S., Cheong G.W., Yun D.J., et al. 2004. Two enzymes in one: Two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell. 117, 625–635.

    Article  CAS  PubMed  Google Scholar 

  35. Lee W., Choi K.S., Riddell J., Ip C., Ghosh D., Park J.H., Park Y.M. 2007. Human peroxiredoxin 1 and 2 are not duplicate proteins: the unique presence of CYS83 in Prx1 underscores the structural and functional differences between Prx1 and Prx2. J. Biol. Chem. 282, 22011–22022.

    Article  CAS  PubMed  Google Scholar 

  36. Yan Y., Sabharwal P., Rao M., Sockanathan S. 2009. The antioxidant enzyme Prdx1 controls neuronal differentiation by thiol-redox-dependent activation of GDE2. Cell. 138, 1209–1221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Rao M., Sockanathan S. 2005. Transmembrane protein GDE2 induces motor neuron differentiation in vivo. Science. 309, 2212–2215.

    Article  CAS  PubMed  Google Scholar 

  38. Yanaka N. 2007. Mammalian glycerophosphodiester phosphodiesterases. Biosci. Biotechnol. Biochem. 71, 1811–1818.

    Article  CAS  PubMed  Google Scholar 

  39. Cao J., Schulte J., Knight A., Leslie N.R., Zagozdzon A., Bronson R., Manevich Y., Beeson C., Neumann C.A. 2009. Prdx1 inhibits tumorigenesis via regulating PTEN/AKT activity. EMBO J. 28, 1505–1517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Egler R.A., Fernandes E., Rothermund K., Sereika S., de Souza-Pinto N., Jaruga P., Dizdaroglu M., Prochownik E.V. 2005. Regulation of reactive oxygen species, DNA damage, and c-Myc function by peroxiredoxin 1. Oncogene. 24, 8038–8050.

    Article  CAS  PubMed  Google Scholar 

  41. Kim S.Y., Kim T.J., Lee K.Y. 2008. A novel function of peroxiredoxin 1 (Prx-1) in apoptosis signal-regulating kinase 1 (ASKl)-mediated signaling pathway. FEBS Lett. 582, 1913–1918.

    Article  CAS  PubMed  Google Scholar 

  42. Gertz M., Fischer F., Leipelt M., Wolters D., Steegborn C. 2009. Identification of peroxiredoxin 1 as a novel interaction partner for the lifespan regulator protein p66Shc. Aging (Albany, NY). 1, 254–265.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Adler V., Yin Z., Fuchs S.Y., Benezra M., Rosario L., Tew K.D., Pincus M.R., Sardana M., Henderson C.J., Wolf C.R., Davis R.J., Ronai Z. 1999. Regulation of JNK signaling by GSTp. EMBO J. 18, 1321–1334.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Riddell J.R., Wang X.Y., Minderman H., Gollnick S.O. 2010. Peroxiredoxin 1 stimulates secretion of proinflammatory cytokines by binding to TLR4. J. Immunol. 184, 1022–1030.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Riddell J.R., Bshara W., Moser M.T., Spernyak J.A., Foster B.A., Gollnick S.O. 2011. Peroxiredoxin 1 controls prostate cancer growth through Toll-like receptor 4-dependent regulation of tumor vasculature. Cancer Res. 71, 1–10.

    Article  Google Scholar 

  46. Ishii T., Warabi E., Yanagawa T. 2012. Novel roles of peroxiredoxins in inflammation, cancer and innate immunity. J. Clin. Biochem. Nutr. 50, 91–105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Cell Biophysics, Russian Academy of Sciences, Pushchino, Moscow region, 142290, Russia

    M. G. Sharapov, V. I. Novoselov & V. K. Ravin

Authors
  1. M. G. Sharapov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. I. Novoselov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. K. Ravin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. G. Sharapov.

Additional information

Original Russian Text © M.G. Sharapov, V.I. Novoselov, V.K. Ravin, 2016, published in Molekulyarnaya Biologiya, 2016, Vol. 50, No. 2, pp. 336–346.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharapov, M.G., Novoselov, V.I. & Ravin, V.K. Xenopus laevis peroxiredoxins: Gene expression during development and characterization of the enzymes. Mol Biol 50, 292–301 (2016). https://doi.org/10.1134/S0026893316020217

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893316020217

Keywords

Search

Navigation