Advertisement

Peroxiredoxins in Gametogenesis and Embryo Development

  • Isabelle Donnay
  • Bernard Knoops
Part of the Subcellular Biochemistry book series (SCBI, volume 44)

Abstract

Reactive oxygen species have been implicated in gametogenesis and embryo development in animals. As peroxiredoxins are now recognized as important protective antioxidant enzymes as well as modulators of hydrogen peroxide-mediated signaling, we addressed here the putative role of this novel family of peroxidases in gamete maturation and during embryogenesis in mammals and insects

Keywords

Gametogenesis Embryogenesis Mammals Insects Reactive oxygen species Apoptosis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agarwal, A., Gupta S., Sharma R.K., 2005, Role of oxidative stress in female reproduction. Reprod. Biol. Endocrinol. 3: 28.CrossRefPubMedGoogle Scholar
  2. Baker, M.A., Aitken R.J., 2004, The importance of redox regulated pathways in sperm cell biology. Mol. Cell. Endocrinol. 216: 47–54.CrossRefPubMedGoogle Scholar
  3. Baker, M.A., Krutskikh A., Curry B.J., Hetherington L., Aitken R.J., 2005, Identification of cytochrome-b5 reductase as the enzyme responsible for NADH-dependent lucigenin chemiluminescence in human spermatozoa. Biol. Reprod. 73: 334–342.CrossRefPubMedGoogle Scholar
  4. Blondin, P., Coenen K., Sirard M.A., 1997, The impact of reactive oxygen species on bovine sperm fertilizing ability and oocyte maturation. J. Androl. 18: 454–460.PubMedGoogle Scholar
  5. Borchert, A., Wang C.C., Ufer C., Schiebel H., Savaskan N.E., Kühn, H., 2006, The role of phospholipid hydroperoxide glutathione peroxidase (GPx4) isoforms in murine embryogenesis. J. Biol. Chem. 281: 19655–19664.CrossRefPubMedGoogle Scholar
  6. Chaube, S.K., Prasad P.V., Thakur S.C., Shrivastav T.G., 2005, Hydrogen peroxide modulates meiotic cell cycle and induces morphological features characteristic of apoptosis in rat oocytes cultured in vitro. Apoptosis 10: 863–874.CrossRefPubMedGoogle Scholar
  7. Chu, S.H., Lee-Kang J., Lee K.H., Lee, K., 2003, Roles of reactive oxygen species, NF-kappaB, and peroxiredoxins in glycochenodeoxycholic acid-induced rat hepatocytes death. Pharmacology 69: 12–19.CrossRefPubMedGoogle Scholar
  8. Das, K.C., Pahl P.M., Guo X.L., White, C.W., 2001, Induction of peroxiredoxin gene expression by oxygen in lungs of newborn primates. Am. J Respir. Cell. Mol. Biol 25: 226–232.PubMedGoogle Scholar
  9. Dekel, N., 2005, Cellular, biochemical and molecular mechanisms regulating oocyte maturation. Mol. Cell. Endocrinol. 234: 19–25.CrossRefPubMedGoogle Scholar
  10. Ellederova, Z., Halada, P., Man, P., Kubelka, M., Motlik, J., Kovarova, H., 2004, Protein patterns of pig oocytes during in vitro maturation. Biol. Reprod. 71: 1533–1539.CrossRefPubMedGoogle Scholar
  11. Fouchecourt, S., Metayer S., Locatelli A., Dacheux F., Dacheux J.L., 2000, Stallion epididymal fluid proteome: qualitative and quantitative characterization; secretion and dynamic changes of major proteins. Biol. Reprod. 62: 1790–1803.CrossRefPubMedGoogle Scholar
  12. Guerin, P., El Mouatassim, S., Menezo, Y., 2001, Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7: 175–189.CrossRefPubMedGoogle Scholar
  13. Harvey, M.B., Arcellana-Panlilio, M.Y., Zhang, X., Schultz, G.A., Watson, A.J., 1995, Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture. Biol. Reprod. 53: 532–540.CrossRefPubMedGoogle Scholar
  14. Hinton, B.T., Palladino, M.A., Rudolph, D., Labus, J.C., 1995, The epididymis as protector of maturing spermatozoa. Reprod. Fertil. Dev. 7: 731–745.CrossRefPubMedGoogle Scholar
  15. Hoang, V.M., Foulk R., Clauser, K., Burlingame, A., Gibson, B.W., Fisher, S.J., 2001, Functional proteomics: examining the effects of hypoxia on the cytotrophoblast protein repertoire. Biochemistry 40: 4077–4086.CrossRefPubMedGoogle Scholar
  16. Jervis, K.M., Robaire, B., 2001, Dynamic changes in gene expression along the rat epididymis. Biol. Reprod. 65: 696–703.CrossRefPubMedGoogle Scholar
  17. Kanzok, S.M., Fechner, A., Bauer, H., Ulschmid, J.K., Muller, H.M., Botella-Munoz, J., Schneuwly, S., Schirmer, R., Becker, K., 2001, Substitution of the thioredoxin system for glutathione reductase in Drosophila melanogaster. Science 291: 643–646.CrossRefPubMedGoogle Scholar
  18. Kim, H.S., Kang, S.W., Rhee, S.G., Clerch, L.B., 2001, Rat lung peroxiredoxins I and II are differentially regulated during development and by hyperoxia. Am J Physiol Lung Cell. Mol. Physiol. 280: L1212–L1217.PubMedGoogle Scholar
  19. Kim, H.S., Pak, J.H., Gonzales, L.W., Feinstein, S.I., Fisher, A.B., 2002, Regulation of 1-cys peroxiredoxin expression in lung epithelial cells. Am. J. Respir. Cell. Mol. Biol. 27: 227–233.PubMedGoogle Scholar
  20. Lee, K., Park, J.S., Kim, Y.J., Soo Lee, Y.S., Sook Hwang, T.S., Kim, D.J., Park, E.M., Park, Y.M., 2002, Differential expression of Prx I and II in mouse testis and their up-regulation by radiation. Biochem. Biophys. Res. Commun. 296: 337–342.CrossRefPubMedGoogle Scholar
  21. Lee, T.H., Kim, S.U., Yu, S.L., Kim, S.H., Park do, 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.CrossRefPubMedGoogle Scholar
  22. Lee, T.H., Yu, S.L., Kim, S.U., Lee, K.K., Rhee, S.G., Yu, D.Y., 1999, Characterization of mouse peroxiredoxin I genomic DNA and its expression. Gene 239: 243–250.CrossRefPubMedGoogle Scholar
  23. Lequarre, A.S., Feugang, J.M., Malhomme, O., Donnay, I.; Massip, A., Van Langendonckt, A, 2001, Expression of Cu/Zn and Mn superoxide dismutases during bovine embryo development: influence of in vitro culture. Mol. Reprod. Dev. 58: 45–53.CrossRefPubMedGoogle Scholar
  24. Lequarre, A.S., Traverson, J.M., Marchandise, J., Donnay, I., 2004, Poly(A) RNA is reduced by half during bovine oocyte maturation but increases when meiotic arrest is maintained with CDK inhibitors. Biol. Reprod. 71: 425–431.CrossRefPubMedGoogle Scholar
  25. Leyens, G., Donnay, I., 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.CrossRefPubMedGoogle Scholar
  26. Leyens, G., Knoops, B., Donnay, I., 2004a. Expression of peroxiredoxins in bovine oocytes and embryos produced in vitro. Mol Reprod Dev 69: 243–251.CrossRefGoogle Scholar
  27. Leyens, G., Verhaeghe, B., Landtmeters, M., Marchandise, J., Knoops, B., Donnay, I., 2004b, Peroxiredoxin 6 is upregulated in bovine oocytes and cumulus cells during in vitro maturation: role of intercellular communication. Biol. Reprod. 71: 1646–1651.CrossRefGoogle Scholar
  28. Lim, M.J., Chae, H.Z., Rhee, S.G., Yu, D.Y., Lee, K.K., Yeom, Y.I., 1998, The type II peroxiredoxin gene family of the mouse: molecular structure, expression and evolution. Gene 216: 197–205.CrossRefPubMedGoogle Scholar
  29. Liu, A.X., Jin, F., Zhang, W., Zhou, T.H., Zhou, C.Y., Yao, W.M., Qian, Y.L., and Huang, H.F., 2006, Proteomic Analysis on the Alteration of Protein Expression in the Placental Villous Tissue of Early Pregnancy Loss. Biol. Reprod., May 31 (Epub ahead of print).Google Scholar
  30. MacLeod, J. 1943, The role of oxygen in the metabolism and motility of human spermatozoa. Am. J. Physiol. 138: 512–518.Google Scholar
  31. Maiorino, M., Bosello, V., Ursini, F., Foresta, C., Garolla, A., Scapin, M., Sztajer, H., Flohè, L., 2003, Genetic variations of gpx-4 and male infertility in humans. Biol. Reprod. 68: 1134–1141.CrossRefPubMedGoogle Scholar
  32. Maiorino, M., Ursini, F., Bosello, V., Toppo, S., Toeatto, S. C., Mauri, P., Becker, K., Roveri, A., Bulato, C., Benazzi, L., de Palma, A., and Flohé, L., 2007, The thioredoxin specificity of Drosophila GPx: a paradigm for a peroxiredoxin- like mechanism of many glutathione peroxidases. J. Mol. Biol. 365: 1033–1046.CrossRefPubMedGoogle Scholar
  33. Munks, R.J., Sant’Anna, M.R., Grail, W., Gibson, W., Igglesden, T., Yoshiyama, M., Lehane, S.M., Lehanne, M.J., 2005, Antioxidant gene expression in the blood-feeding fly Glossina morsitans morsitans. Insect. Mol. Biol. 14: 483–491.CrossRefPubMedGoogle Scholar
  34. 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 Prx1 in erythrocyte antioxidant defence and tumour suppression. Nature 424: 561–565.CrossRefPubMedGoogle Scholar
  35. O’Flaherty, C., de Lamirande, E., and Gagnon, C., 2006, Reactive oxygen species modulate independent protein phosphorylation pathways during human sperm capacitation. Free Radic. Biol. Med. 40: 1045–1055.CrossRefPubMedGoogle Scholar
  36. Okado-Matsumoto, A., Matsumoto, A., Fujii, J., Taniguchi, N., 2000, Peroxiredoxin IV is a secretable protein with heparin-binding properties under reduced conditions. J. Biochem. (Tokyo) 127: 493–501.Google Scholar
  37. Pasqualotto, E. B., Agarwal, A., Sharma, R.K., Izzo, V.M., Pinotti, J.A., Joshi, N.J., Rose B.I., 2004, Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil. Steril. 81: 973–976.CrossRefPubMedGoogle Scholar
  38. Peng, Y., Yang, P.H., Guo, Y., Ng, S.S., Liu, J., Fung, P.C., Tay, D., Ge, J., He, M.L., Kung, H.F., Lin, M.C., 2004a, Catalase and peroxiredoxin 5 protect Xenopus embryos against alcohol-induced ocular anomalies. Invest. Ophthalmol. Vis. Sci. 45: 23–29.CrossRefGoogle Scholar
  39. Peng, Y., Yang, P.H., Ng, S.S., Lum, C.T., Kung, H.F., Lin, M.C., 2004b, Protection of Xenopus laevis embryos against alcohol-induced delayed gut maturation and growth retardation by peroxiredoxin 5 and catalase. J Mol Biol 340: 819–827.CrossRefGoogle Scholar
  40. Radyuk, S.N., Klichko, V.I., Spinola, B., Sohal, R.S., Orr, W.C., 2001, The peroxiredoxin gene family in Drosophila melanogaster. Free Radic. Biol. Med. 31: 1090–1100.CrossRefPubMedGoogle Scholar
  41. Rhee, S.G., Kang, S.W., Jeong, W., Chang, T.S., Yang, K.S., Woo, H.A., 2005, Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr. Opin. Cell. Biol. 17: 183–189.CrossRefPubMedGoogle Scholar
  42. Rodriguez, J., Agudo, M., Van Damme, J., Vandekerchove, J., Santaren, J.F., 2000, Polypeptides differentially expressed in imaginal discs define the peroxiredoxin family of genes in Drosophila. Eur. J. Biochem. 267: 487–497.CrossRefPubMedGoogle Scholar
  43. Roveri, A., Ursini, F., Flohe, L., and Maiorino, M., 2001, PHGPx and spermatogenesis. Biofactors 14: 213–222.CrossRefPubMedGoogle Scholar
  44. Sanchez-Font, M.F., Sebastia, J., Sanfeliu, C., Cristofol, R., Marfany, G., Gonzalez-Duarte, R., 2003, Peroxiredoxin 2 (PRX2), an antioxidant enzyme, is under-expressed in Down syndrome fetal brains. Cell. Mol. Life Sci. 60: 1513–1523.CrossRefPubMedGoogle Scholar
  45. Sasagawa, I., Matsuki, S., Suzuki, Y., Iuchi, Y., Tohya, K., Kimura, M., Nakada, T., Fujii, J., 2001, Possible involvement of the membrane-bound form of peroxiredoxin 4 in acrosome formation during spermiogenesis of rats. Eur. J. Biochem. 268: 3053–3061.CrossRefPubMedGoogle Scholar
  46. Schneider, M., Vogt-Weisenhorn, D. M., Seiler, A., Bornkamm, G. W., Brielmeier, M. and Conrad, M., 2006, Embryonic expression profile of phospholipid hydroperoxide glutathione peroxidase. Gene Expr. Patterns 6: 489–494.CrossRefPubMedGoogle Scholar
  47. Seligman, J., Newton, G.L., Faney, R.C., Shalgi, R., Kosower, N.S., 2005, Nonprotein thiols and disulfides in rat epididymal spermatozoa and epididymal fluid: role of gamma-glutamyl-transpeptidase in sperm maturation. J. Androl. 26: 629–637.CrossRefPubMedGoogle Scholar
  48. Shan, S.W., Tank, M.K., Cai, D.Q., Chui, Y.L., Chow, P.H., Grotewold, L., Kee, L.L., 2005, Comparative proteomic analysis identifies protein disulfide isomerase and peroxiredoxin 1 as new players involved in embryonic interdigital cell death. Dev. Dyn. 233: 266–281.CrossRefPubMedGoogle Scholar
  49. Takami, M., Preston, S.L., Toyloy, V.A., Behrman, H.R., 1999, Antioxidants reversibly inhibit the spontaneous resumption of meiosis. Am. J. Physio.l 276: E684–E688.Google Scholar
  50. Tosic, J., Walton, A., 1946, Formation of hydrogen peroxide by spermatozoa and its inhibitory effect on respiration. Nature 158: 485.CrossRefGoogle Scholar
  51. Tramer, F., Rocco, F., Micali, F., Sandri, G., Panfili, E., 1998, Antioxidant systems in rat epididymal spermatozoa. Biol. Reprod. 59: 753–788.CrossRefPubMedGoogle Scholar
  52. Ursini, F., Heim, S., Kiess, M., Maiorino, M., Roveri, A., Wissing, J., Flohe, L., 1999, Dual function of the selenoprotein PHGPx during sperm maturation. Science 285: 1393–1396.CrossRefPubMedGoogle Scholar
  53. 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.CrossRefPubMedGoogle Scholar
  54. Wiener-Megnazi, Z., Vardi, L., Lissak, A., Shinzer, S., Reznick, A.Z., Ishai, D., Lahav-Baratz, S., Shiloh, H., Koifman, M., Dirnfeld, M., 2004, Oxidative stress indices in follicular fluid as measured by the thermochemiluminescence assay correlate with outcome parameters in in vitro fertilization. Fertil. Steril. 82 Suppl 3: 1171–1176.CrossRefPubMedGoogle Scholar
  55. Zini, A., Fisher, M.A., Mak, V., Phang, D., Jarvi, K., 2002, Catalase-like and superoxide dismutase-like activities in human seminal plasma. Urol. Res. 30: 321–323.CrossRefPubMedGoogle Scholar
  56. Zubkova, E.V., Robaire, B., 2004, Effect of glutathione depletion on antioxidant enzymes in the epididymis, seminal vesicles, and liver and on spermatozoa motility in the aging brown Norway rat. Biol. Reprod. 71: 1002–1008.CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Isabelle Donnay
    • 1
  • Bernard Knoops
    • 2
  1. 1.Veterinary Unit, Institut des Sciences de la VieUniversité catholique de LouvainPlace Croix du Sud 5Belgium
  2. 2.Laboratory of Cell Biology, Institut des Sciences de la VieUniversité catholique de LouvainPlace Croix du Sud 5Belgium

Personalised recommendations