The nuclear form of phospholipid hydroperoxide glutathione peroxidase is a protein thiol peroxidase contributing to sperm chromatin stability

Molecular and Cellular Biology

Volumn 25, Issue 17, 2005, Pages 7637-7644

  Conrad, M ^a   Moreno, S G ^a,b   Sinowatz, F ^c   Ursini, F ^d   Kolle S ^c   Roveri, A ^d   Brielmeier, M ^a   Wurst, W ^a   Maiorino, M ^d   Bornkamm, G W ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^c UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACRIDINE ORANGE; BROMOBIMANE; PEROXIDASE; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; PROTEIN THIOL PEROXIDASE; SELENOPROTEIN; TOLONIUM CHLORIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; CYTOSOL; DESICCATION; EPIDIDYMIS; GENE; GENE DELETION; GERM CELL; HISTOPATHOLOGY; HYDRATION; KNOCKOUT MOUSE; MALE; MALE FERTILITY; MITOCHONDRION; MORPHOLOGY; MOUSE; NONHUMAN; OXIDATION; PHGPX GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RODENT; SELENIUM DEFICIENCY; SPERM; SPERMATID; SPERMATOZOON; STAINING; TESTIS; TITRIMETRY;

ANIMALS; CELL NUCLEUS; CELL SHAPE; CHROMATIN; EPITHELIUM; FERTILITY; GLUTATHIONE PEROXIDASE; MALE; MICE; MICE, KNOCKOUT; SPERMATOZOA; SULFHYDRYL COMPOUNDS;

CAPUT; RODENTIA;

EID: 23844508188     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.17.7637-7644.2005     Document Type: Article

References (38)

1. Balhorn, R. 1990. Mammalian protamines: structure and molecular interactions, p. 366-395. In K. W. Adolf (ed.), Molecular biology of chromosome function. Springer Verlag, New York, N.Y.
2. Balhorn, R. 1982. A model for the structure of chromatin in mammalian sperm. J. Cell Biol. 93:298-305.
3. Balhorn, R., M. Corzett, J. Mazrimas, and B. Watkins. 1991. Identification of bull protamine disulfides. Biochemistry 30:175-181.
4. Balhorn, R., M. Corzett, and J. A. Mazrimas. 1992. Formation of intraprotamine disulfides in vitro. Arch. Biochem. Biophys. 296:384-393.
5. Behne, D., H. Weiler, and A. Kyriakopoulos. 1996. Effects of selenium deficiency on testicular morphology and function in rats. J. Reprod. Fertil. 106:291-297.
6. Brewer, L., M. Corzett, and R. Balhorn. 2002. Condensation of DNA by spermatid basic nuclear proteins. J. Biol. Chem. 277:38895-38900.
7. Brewer, L. R., M. Corzett, and R. Balhorn. 1999. Protamine-induced condensation and decondensation of the same DNA molecule. Science 286:120-123.
8. Cho, C., W. D. Willis, E. H. Goulding, H. Jung-Ha, Y. C. Choi, N. B. Hecht, and E. M. Eddy. 2001. Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat. Genet. 28:82-86.
9. Conrad, M., M. Brielmeier, W. Wurst, and G. W. Bornkamm. 2003. Optimized vector for conditional gene targeting in mouse embryonic stem cells. BioTechniques 34:1136-1138, 1140.
10. Conrad, M., C. Jakupoglu, S. G. Moreno, S. Lippl, A. Banjac, M. Schneider, H. Beck, A. K. Hatzopoulos, U. Just, F. Sinowatz, W. Schmahl, K. R. Chien, W. Wurst, G. W. Bornkamm, and M. Brielmeier. 2004. Essential role for mitochondrial thioredoxin reductase in hematopoiesis, heart development, and heart function. Mol. Cell. Biol. 24:9414-9423.
11. Erenpreisa, J., T. Freivalds, H. Roach, and R. Alston. 1997. Apoptotic cell nuclei favour aggregation and fluorescence quenching of DNA dyes. Histochem. Cell Biol. 108:67-75.
12. Erenpreiss, J., J. Bars, V. Lipatnikova, J. Erenpreisa, and J. Zalkalns. 2001. Comparative study of cytochemical tests for sperm chromatin integrity. J. Androl. 22:45-53.
13. Godeas, C., F. Tramer, F. Micali, M. Soranzo, G. Sandri, and E. Panfili. 1997. Distribution and possible novel role of phospholipid hydroperoxide glutathione peroxidase in rat epididymal spermatozoa. Biol. Reprod. 57: 1502-1508.
14. Imai, H., F. Hirao, T. Sakamoto, K. Sekine, Y. Mizukura, M. Saito, T. Kitamoto, M. Hayasaka, K. Hanaoka, and Y. Nakagawa. 2003. Early embryonic lethality caused by targeted disruption of the mouse PHOPx gene. Biochem. Biophys. Res. Commun. 305:278-286.
15. Joyner, A. L. 2000. Gene targeting-a practical approach, 2nd ed. Oxford University Press, New York, N.Y.
16. Knopp, E. A., T. L. Arndt, K. L. Eng, M. Caldwell, R. C. LeBoeuf, S. S. Deeb, and K. D. O'Brien. 1999. Murine phospholipid hydroperoxide glutathione peroxidase: cDNA sequence, tissue expression, and mapping. Mamm. Genome 10:601-605.
17. Kosower, N. S., and E. M. Kosower. 1987. Thiol labeling with bromobimanes. Methods Enzymol. 143:76-84.
18. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
19. Maiorino, M., P. Mauri, A. Roveri, L. Benazzi, S. Toppo, V. Bosello, and F. Ursini. 2005. Primary structure of the nuclear forms of phospholipid hydroperoxide glutathione peroxidase (PHGPx) in rat spermatozoa. FEBS Lett. 579:667-670.
20. Maiorino, M., M. Scapin, F. Ursini, M. Biasolo, V. Bosello, and L. Flohe. 2003. Distinct promoters determine alternative transcription of gpx-4 into phospholipid-hydroperoxide glutathione peroxidase variants. J. Biol. Chem. 278:34286-34290.
21. Maiorino, M., J. B. Wissing, R. Brigelius-Flohe, F. Calabrese, A. Roveri, P. Steinert, F. Ursini, and L. Flohe. 1998. Testosterone mediates expression of the selenoprotein PHGPx by induction of spermatogenesis and not by direct transcriptional gene activation. FASEB J. 12:1359-1370.
22. Mauri, P., L. Benazzi, L. Flohe, M. Maiorino, P. G. Pietta, S. Pilawa, A. Roveri, and F. Ursini. 2003. Versatility of selenium catalysis in PHGPx unraveled by LC/ESI-MS/MS. Biol. Chem. 384:575-588.
23. Moreno, S. G., G. Laux, M. Brielmeier, G. W. Bornkamm, and M. Conrad. 2003. Testis-specific expression of the nuclear form of phospholipid hydroperoxide glutathione peroxidase (PHGPx). Biol. Chem. 384:635-643.
24. Pfeifer, H., M. Conrad, D. Roethlein, A. Kyriakopoulos, M. Brielmeier, G. W. Bornkamm, and D. Behne. 2001. Identification of a specific sperm nuclei selenoenzyme necessary for protamine thiol cross-linking during sperm maturation. FASEB J. 15:1236-1238.
25. Pushpa-Rekha, T. R., A. L. Burdsall, L. M. Oleksa, G. M. Chisolm, and D. M. Driscoll. 1995. Rat phospholipid-hydroperoxide glutathione peroxidase. cDNA cloning and identification of multiple transcription and translation start sites. J. Biol. Chem. 270:26993-26999.
26. Rousseaux, J., and R. Rousseaux-Prevost. 1995. Molecular localization of free thiols in human sperm chromatin. Biol. Reprod. 52:1066-1072.
27. Roveri, A., M. Maiorino, and F. Ursini. 1994. Enzymatic and immunological measurements of soluble and membrane-bound phospholipid-hydroperoxide glutathione peroxidase. Methods Enzymol. 233:202-212.
28. Roveri, A., F. Ursini, L. Flohe, and M. Maiorino. 2001. PHGPx and spermatogenesis. Biofactors 14:213-222.
29. Sega, G. A., R. P. Alcota, C. P. Tancongco, and P. A. Brimer. 1989. Acrylamide binding to the DNA and protamine of spermiogenic stages in the mouse and its relationship to genetic damage. Mutat. Res. 216:221-230.
30. Shalgi, R., J. Seligman, and N. S. Kosower. 1989. Dynamics of the thiol status of rat spermatozoa during maturation: analysis with the fluorescent labeling agent monobromobimane. Biol. Reprod. 40:1037-1045.
31. 29a. Shelby, M. D., K. T. Cain, L. A. Hughes, P. W. Braden, and W. M. Generoso. 1986. Dominant lethal effects of acrylamide in male mice. Mutat. Res. 173: 35-40.
32. Shi, S. R., M. E. Key, and K. L. Kalra. 1991. Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J. Histochem. Cytochem. 39:741-748.
33. Ursini, F., S. Heim, M. Kiess, M. Maiorino, A. Roveri, J. Wissing, and L. Flohe. 1999. Dual function of the selenoprotein PHGPx during sperm maturation. Science 285:1393-1396.
34. Ursini, F., M. Maiorino, R. Brigelius-Flohe, K. D. Aumann, A. Roveri, D. Schomburg, and L. Flohe. 1995. Diversity of glutathione peroxidases. Methods Enzymol. 252:38-53.
35. Ursini, F., M. Maiorino, M. Valente, L. Ferri, and C. Gregolin. 1982. Purification from pig liver of a protein which protects liposomes and biomembranes from peroxidative degradation and exhibits glutathione peroxidase activity on phosphatidylcholine hydroperoxides. Biochim. Biophys. Acta 710: 197-211.
36. Watanabe, T., and A. Endo. 1991. Effects of selenium deficiency on sperm morphology and spermatocyte chromosomes in mice. Mutat. Res. 262:93-99.
37. Weis, K. 1998. Importins and exportins: how to get in and out of the nucleus. Trends Biochem. Sci. 23:185-189.
38. Yant, L. J., Q. Ran, L. Rao, H. Van Remmen, T. Shibatani, J. G. Belter, L. Motta, A. Richardson, and T. A. Prolla. 2003. The selenoprotein GPX4 is essential for mouse development and protects from radiation and oxidative damage insults. Free Radic. Biol. Med. 34:496-502.