Testosterone mediates expression of the selenoprotein PHGPx by induction of spermatogenesis and not by direct transcriptional gene activation

FASEB Journal

Volumn 12, Issue 13, 1998, Pages 1359-1370

  Maiorino, Matilde ^a   Wissing, Josef B ^d   Brigelius Flohé, Regina ^c   Calabrese, Fiorella ^b   Roveri, Antonella ^a   Steinert, Peter ^d   Ursini, Fulvio ^a   Flohé, Leopold ^d  

^a Dipartimento di Chimica Biologica   (Italy)

^b Istituto di Anatomia Umana Normale   (Italy)

^c GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^d TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Glutathione peroxidases; Selenium

Indexed keywords

CHORIONIC GONADOTROPIN; ETHYLENE GLYCOL DIMESYLATE; FORSKOLIN; GLUTATHIONE PEROXIDASE; MESSENGER RNA; SELENIUM; SELENOPROTEIN; TESTOSTERONE;

AGE; ANIMAL TISSUE; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; ENZYME ACTIVITY; GENE ACTIVATION; IN SITU HYBRIDIZATION; LEYDIG CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEXUAL MATURATION; SPERMATID; SPERMATOGENESIS; TESTIS FUNCTION; TRANSCRIPTION REGULATION;

EID: 0031689441     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.12.13.1359     Document Type: Article

References (52)

1. Behne, D., Hofer, T., von Berswordt Wallrabe, R., and Egler, W. (1982) Selenium in the testis of the rat: studies on its regulation and its importance for the organism. J. Nutr. 112, 1682-1687
2. Wallace, E., Calvin, H .I., Ploeu, K., and Cooper, G. W. (1987) Functional and developmental studies on the role of selenium in spermatogenesis. In Selenium in Biology and Medicine (Combs, G. F., Levander, O. A., Spallholz, J. E., Oldfield, J. E., eds) Part A, pp. 181-196, AVI Publishing Co., Westport, Connecticut
3. Behne, D., Weiler, H., and Kyriakopoulos, A. (1996) Effects of selenium deficiency on testicular morphology and function in rats. J. Reprod. Fertil. 106, 291-297
4. Brown, D. G., and Burk, R. F. (1973) Selenium retention in tissues and sperm of rats fed a torula yeast diet. J. Nutr. 103, 102-108
5. Wu., A. S. H., Oldfield J. E., Whanger P. D., and Weiswig, P. H. (1973) Effects of selenium, vitamin E, and antioxidants on testicular function in rats. Biol Reprod. 8, 625-629
6. Wu, A. S. H., Oldfield, J. E., Shull, L. R., and Checke, P. R. (1979) Specific effect of selenium deficiency on rat sperm. Biol. Reprod. 20, 793, 798
7. Bock, A., Forchhammer, K., Heider, J., and Baron, C. (1991) Selenoprotein synthesis: An expansion of the genetic code. Trends Biol. Sci. 16, 463-467
8. Behne, D., Weiss-Nowak, C., Kalcklösch, M., Westphal, C., Gessner, H., and Kyriakopoulos, A. (1994) Applications of nuclear analytical methods in the investigation and identification of new selenoproteins. Biol. Trace Elem. Res. 43/45, 287-298
9. Flohe, L., Günzler, W. A., and Schock, H. H. (1973) Glutathione peroxidase: a selenoenzyme. FEBS Lett. 32, 132-134
10. Rotruck, J. T., Pope, A. L., Ganther, H. E., Swanson, A. B., Hafeman, D. G., and Hoekstra, W.G. (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179, 588-590
11. Brigelius-Flohé, R., Aumann, K.-D., Blöcker, H., Gross, G., Kiess, M., Klöppel, K.-D., Maiorino, M., Roved, A., Schuckelt, R., Ursini, F., Wingender, E., and Flohé, L. (1994) Phospholipid-hydroperoxide glutathione peroxidase: genomic DNA, cDNA, and deduced amino acid sequence. J. Biol. Chem. 269, 7342-7348
12. Takahashi, K., Akasaka, M., Yamamoto, Y., Kobayashi, C., Mizoguchi, J., and Koyama, J. (1990) Primary structure of human plasma glutathione peroxidase deduced from cDNA sequences. J. Biochem. (Tokyo) 108, 145-158
13. Chu, F. F., Esworthy, R. S., Ho, V.-S., Bermeister, M., Swiderik, K., and Elliott, R. W. (1997) Expression and chromosomal mapping of mouse Gpx2 gene encoding the gastrointestinal form of glutathione peroxidase, GPx-gi. Biomed. Environ. Sci. 10, 156-162
14. Ursini, F., Maiorino, M., Brigelius-Flohé, R., Aumann, K. D., Roveri, A., Schomburg, D., and Flohé, L. (1995) The diversity of glutathione peroxidases. Methods Enzymol, 252, 38-53
15. Behne, D., Kyriakopoulos, A., Meinhold, H., and Köhrle, J. (1990) Identification of type I iodothyronine 5′-deiodinase as a selenoenzyme. Biochem. Biophys. Res. Commun. 173, 1143-1149
16. Berry, M. J., Banu, L., and Larsen, P. R. (1991) Type I iodothironine deiodinase is a selenocysteine-containing enzyme Nature (London) 349, 438-440
17. Croteau, W., Whittemore, S. L., Schneider, M. J., and Germain, D. L. S. (1995) Cloning and expression of a cDNA for mammalian type III iodothyronine deiodinase. J. Biol. Chem. 270, 16569-16575
18. Tamura, T., and Stadtman, T.C. (1996) A new selenoprotein from human lung adenocarcinoma cells: purification, properties, and thioredoxin reductase activity. Proc. Natl. Acad. Sci. USA 93, 1006-1011
19. Guimaraes, M. J., Peterson, D., Vicari, A., Cocks, B. G., Copeland, N.G., Gilbert, D. J., Jenkins, N. A., Ferrick, D. A., Kastelein, R., Bazan, J. F., and Zlotnic, A. (1996) Identification of a novel SelD homolg from eukaryotes, bacteria, and archaea: is there an autoregolatory mechanism in selenocysteine metabolism? Proc. Natl. Acad. Sci. USA 93, 15086-15091
20. Rocher, C., Lalanne, J. L., and Chaudiere, J. (1992) Purification and properties of a recombinant sulfur analog of murine selenium-glutathione peroxidase. Eur. J. Biochem. 205, 955-60
21. Maiorino, M., Aumann, K.-D., Brigelius-Flohé, R., Doria, D., den Heuvel, J. v., McCarthy, J., Roveri, A., Ursini, F., and Flohé, L. (1995) Probing the presumed catalytic triad of selenium-containing peroxidases by mutational analysis of phospholipid hydroperoxide glutathione peroxidase (PHGPx). Biol. Chem. Hoppe-Seyler 376, 651-660
22. Berry, M. J., Maia A. L., Kieffer J. D., Harney J. W., and Larsen, P. R. (1992) Substitution of cysteine for selenocysteine in type I iodothyronine deiodinase reduces the catalytic efficiency of the protein but enhances its translation. Endocrinol. 131, 1848-1852
23. Marcocci, L., Flohé, L., and Packer, L. (1997) Evidence for a functional relevance of the selenocysteine residue in mammalian thioredoxin reductase. BioFactors 6, 351-358
24. Stadtman, T. C. (1990) Selenium biochemistry. Annu. Rev. Biochem. 599, 111-127
25. Flohe, L., Wingender, E., and Brigelius-Flohé, R. (1997) The regulation of glutathione peroxidases. In Oxidative Stress and Signal Transduction (Forman, H. J., and Cadenas, E., eds) pp. 415-440, Chapman & Hall, New York
26. Peltola, V., Huhtaniemi, I., Metsa-Ketela, T., and Ahotupa, M. (1996) Induction of lipid peroxidation during steroidogenesis in the rat testis. Endocrinology 137, 105-112
27. Lei, X. G., Everson, J. K., Thompson, K. M., und Sunde, R. A. (1995) Glutathione peroxidase and phospholipid hydroperoxide glutathione peroxidase are differently regulated in rats by dietary selenium. J. Nutr. 125, 1438-1446
28. Roveri, A., Casasco, A., Maiorino, M., Dalan, P., Calligaro, A., and Ursini, F. (1992) Phospholipid hydroperoxide glutathione peroxidase of rat testis: Gonadotropin dependency and immunocytochemical identification. J. Biol. Chem. 267, 6142-6146
29. Pushpa Rekha, T., Burdsal, L. M., Chisolm, G. M., and Driscoll, D. M. (1995) Rat phospholipid-hydroperoxide glutathione peroxidase: cDNA cloning and identification of mulktiple transcription and translation sites. J. Biol. Chem. 270, 26993-26999
30. Maniatis, T., Fritsch, E. F., and Sambrook, J. (1989) In Molecular Cloning. A Laboratory Manual. Cold Spring Harbour Laboratory Press, Cold Spring Harbour, N.Y
31. Jackson, C.-M., and Jackson, H. (1984) Comparative protective actions of gonadotropins and testosterone against the antispermatogenic action of ethane dimethane suphonate. J. Reprod. Fertil. 71, 393-401
32. Besandoun, A., and Weinstein, D. (1976) Assay of proteins in the presence of interfering materials. Anal. Biochem. 70, 241-250
33. Maiorino, M., Gregolin, C., and Ursini, F. (1990) Phospholipid hydroperoxide glutathione peroxidase. Methods Enzymol. 186, 448-457
34. Meyer, E. H. H., Forsgren, K., von Deimling, O., and Engel, W. (1974) Induction of nonspecific carboxyl esterase in the immature rat testis by human chorionic gonadotropin. Endocrinology 95, 1737-1739
35. Chambers, I., Frampton, J., Goldfarb, P., Affara, N., McBain, W., and Harrison, P. R. (1986) The structure of the mouse glutathione peroxidase gene: the selenocysteine in the active site is encoded by the 'termination' codon, TGA. EMBO J. 5, 1221-1227
36. Cusan, L.-C., Pelletier, G., Belanger, A., Seguin, C., Kelly, P.-A., and Labrie, F. (1982) Inhibition of spermatogenesis and steroidogenesis during long term treatment with hCG in the rat. J. Androl. 3, 124-133
37. Kerr, J. B., and Sharpe, R. M. (1989) Focal distinction of spermatogenesis in the testis of adult rats after a single administration of human chorionic gonadotropin. Cell Tissue Res. 257, 163-169
38. Sharpe, R. M., Maddocks, S., and Kerr, J. B. (1990) Cell-cell interactions in the control of spermatogenesis as studied using Leydig cell destruction and testosterone replacement. Am. J. Anat. 188, 3-20
39. Cheng, W. H., Ho, Y.-S., Ross, D. A., Valentine, B. A., Combs, G. F., Jr., and Lei, X. G. (1997) Cellular glutathine peroxidase knockout mice express normal levels of selenium-dependent plasma and phospholipid hydroperoxide glutathione peroxidase in various tissues. J. Nutr. 127, 1445-1450
40. Lei, X. G., Cheng, W. H., Ho, Y. S., Valentine, B. A., Combs, G. F., Jr., and Ross, D. A. (1997) Cellular glutathione peroxidase is the metabolic form of body selenium to protect mice against paraquat lethality. FASEB J. 11, A235
41. Zhang, L., Maiorino, M., Roveri, A., and Ursini, F. (1989) Phospholipid hydroperoxide glutathione peroxidase: specific activity in tissues or rats of different age and comparison with other glutathione peroxidases. Biochim. Biophys. Acta 1006, 140-143
42. Weitzel, F., Ursini, F., and Wendel, A. (1990) Phospholipid hydroperoxide glutathione peroxidase in various mouse organs during selenium deficiency and repletion. Biochim. Biophys. Acta 1036, 88-94
43. Maiorino, M., Roche, C., Kiess, M., Koenig, K., Gawlik, D., Matthes, M., Naldini, E., Pierce, R., and Flohé, L. (1996) A selenium-containing phospholipid hydroperoxide glutathione peroxidase in Schistosoma mansoni. Eur. J. Biochem. 238, 838-844
44. Maiorino, M., Pierce, R., and Flohé, L. (1997) Product of the Schistosoma mansoni glutathione peroxidase gene is a selenium containing phospholipid hydroperoxide glutathione peroxidase (PHGPx) sharing molecular weight and substrate specificity with its mammalian counterpart. Biomed. Environ. Sci. 10, 209-213
45. Roveri, A., Maiorino, M., and Ursini, F. (1994) Enzymatic and immunological measurements of soluble and membrane-bound PHGPx. Methods Enzymol. 233, 202-212
46. Schnurr, K., Belkner, J., Ursini, F., Schewe, T., and Kuhn, H. (1996) The selenoenzyme phospholipid hydroperoxide glutathione peroxidase controls the activity of the 15-lipoxygenase with complex substrates and preserves the specificity of the oxygenation products. J. Biol. Chem. 271, 4653-4658
47. Rapoport, S. M., and Schewe, T. (1986) The maturational breakdown of mitochondria in reticulocytes. Biochim. Biophys. Acta 864, 471-495
48. Weitzel, F., and Wendel, A. (1993) Selenoenzymes regulate the activity of leukocyte 5-lipoxygenase via the peroxide tone. J. Biol. Chem. 268, 6288-6292
49. Brigelius-Flohé, R., Friedrichs, B., Maurer, S., Schultz, M., and Streicher, R. (1997) IL-1 induced NFκB activation is inhibited by overexpression of PHGPx in a human endothelial cell line. Biochem. J. In press
50. Follman, H., and Haberlein, I. (1996) Thioredoxins: universal, yet specific thiol-disulfide redox cofactors. BioFactors 5, 147-150
51. Steinert, P., Bächner, D., and Flohe, L. (1998) Analysis of the mouse Selenoprotein P gene. Biol. Chem. In press
52. Behne, D., Kyriakopoulos, A., Kalcklösch, M., Weiss-Nowak, C., Pfeifer, H., Gessner, H., and Hammel, C. (1997) Two new selenoproteins fond in the prostate glandular epithelium and in the spermatid nuclei. Biomed. Environ. Sci. 10, 340-345