The nuclear form of glutathione peroxidase 4 is associated with sperm nuclear matrix and is required for proper paternal chromatin decondensation at fertilization

Journal of Cellular Physiology

Volumn 227, Issue 4, 2012, Pages 1420-1427

  Puglisi, Rossella ^a   Maccari, Irene ^a   Pipolo, Simona ^a   Conrad, Marcus ^b   Mangia, Franco ^a   Boitani, Carla ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); LAMIN B; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; TOPOISOMERASE 2BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL MATURATION; CELL NUCLEUS; CELL NUCLEUS MATRIX; CELL STRAIN COS1; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN CONDENSATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENZYME LOCALIZATION; EPIDIDYMIS TAIL; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; GERM CELL; HEAD; IMMUNOBLOTTING; IN VITRO STUDY; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; SPERM; WILD TYPE;

ANIMALS; CERCOPITHECUS AETHIOPS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL INSTABILITY; COS CELLS; EMBRYONIC DEVELOPMENT; EPIDIDYMIS; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; GLUTATHIONE PEROXIDASE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR MATRIX; OOCYTES; RECOMBINANT PROTEINS; SPERMATOGENESIS; SPERMATOZOA; TRANSFECTION;

MUS;

EID: 84855719823     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22857     Document Type: Article

References (42)

1. Bertelsmann H, Kuehbacher M, Weseloh G, Kyriakopoulos A, Behne D. 2007. Sperm nuclei glutathione peroxidases and their occurrence in animal species with cysteine-containing protamines. Biochim Biophys Acta 1770:1459-1467.
2. Boitani C, Geremia R, Rossi R, Monesi V. 1980. Electrophoretic pattern of polypeptide synthesis in spermatocytes and spermatids of the mouse. Cell Differ 9:41-49.
3. Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ, Roloff TC, Beisel C, Schubeler D, Stadler MB, Peters AH. 2010. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol 17:679-687.
4. Buffone MG, Foster JA, Gerton GL. 2008. The role of the acrosomal matrix in fertilization. Int J Dev Biol 52:511-522.
5. Conover JC, Gwatkin RB. 1988. Pre-loading of mouse oocytes with DNA-specific fluorochrome (Hoechst 33342) permits rapid detection of sperm-oocyte fusion. J Reprod Fertil 82:681-690.
6. Conrad M, Moreno SG, Sinowatz F, Ursini F, Kolle S, Roveri A, Brielmeier M, Wurst W, Maiorino M, Bornkamm GW. 2005. The nuclear form of phospholipid hydroperoxide glutathione peroxidase is a protein thiol peroxidase contributing to sperm chromatin stability. Mol Cell Biol 25:7637-7644.
7. Godeas C, Tramer F, Micali F, Soranzo M, Sandri G, Panfili E. 1997. Distribution and possible novel role of phospholipid hydroperoxide glutathione peroxidase in rat epididymal spermatozoa. Biol Reprod 57:1502-1508.
8. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. 2009. Distinctive chromatin in human sperm packages genes for embryo development. Nature 460:473-478.
9. Haraguchi CM, Mabuchi T, Hirata S, Shoda T, Yamada AT, Hoshi K, Yokota S. 2003. Spatiotemporal changes of levels of a moonlighting protein, phospholipid hydroperoxide glutathione peroxidase, in subcellular compartments during spermatogenesis in the rat testis. Biol Reprod 69:885-895.
10. Johnson GD, Lalancette C, Linnemann AK, Leduc F, Boissonneault G, Krawetz SA. 2011. The sperm nucleus: Chromatin, RNA, and the nuclear matrix. Reproduction 141:21-36.
11. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
12. Liang H, Yoo SE, Na R, Walter CA, Richardson A, Ran Q. 2009. Short form glutathione peroxidase 4 is the essential isoform required for survival and somatic mitochondrial functions. J Biol Chem 284:30836-30844.
13. Maiorino M, Mauri P, Roveri A, Benazzi L, Toppo S, Bosello V, Ursini F. 2005. Primary structure of the nuclear forms of phospholipid hydroperoxide glutathione peroxidase (PHGPx) in rat spermatozoa. FEBS Lett 579:667-670.
14. Mauri P, Benazzi L, Flohe L, Maiorino M, Pietta PG, Pilawa S, Roveri A, Ursini F. 2003. Versatility of selenium catalysis in PHGPx unraveled by LC/ESI-MS/MS. Biol Chem 384:575-588.
15. Mayer JF, Jr., Chang TS, Zirkin BR. 1981. Spermatogenesis in the mouse 2. Amino acid incorporation into basic nucleoproteins of mouse spermatids and spermatozoa. Biol Reprod 25:1041-1051.
16. McLay DW, Clarke HJ. 2003. Remodelling the paternal chromatin at fertilization in mammals. Reproduction 125:625-633.
17. Meistrich ML. 1989. Histone and basic nuclear protein transitions in mammalian spermatogenesis. In: Hnilica S, Stein GS, Stein JL, editors. Histones and other basic nuclear proteins. Orlando, FL: CRC Press. pp 165-182.
18. Moreno SG, Laux G, Brielmeier M, Bornkamm GW, Conrad M. 2003. Testis-specific expression of the nuclear form of phospholipid hydroperoxide glutathione peroxidase (PHGPx). Biol Chem 384:635-643.
19. Perreault SD, Wolff RA, Zirkin BR. 1984. The role of disulfide bond reduction during mammalian sperm nuclear decondensation in vivo. Dev Biol 101:160-167.
20. Perreault SD, Barbee RR, Slott VL. 1988. Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev Biol 125:181-186.
21. Pfeifer H, Conrad M, Roethlein D, Kyriakopoulos A, Brielmeier M, Bornkamm GW, Behne D. 2001. Identification of a specific sperm nuclei selenoenzyme necessary for protamine thiol cross-linking during sperm maturation. FASEB J 15:1236-1238.
22. Platz RD, Meistrich ML, Grimes SR, Jr. 1977. Low-molecular-weight basic proteins in spermatids. Methods Cell Biol 16:297-316.
23. Puglisi R, Tramer F, Panfili E, Micali F, Sandri G, Boitani C. 2003. Differential splicing of the phospholipid hydroperoxide glutathione peroxidase gene in diploid and haploid male germ cells in the rat. Biol Reprod 68:405-411.
24. Quinn P, Barros C, Whittingham DG. 1982. Preservation of hamster oocytes to assay the fertilizing capacity of human spermatozoa. J Reprod Fertil 66:161-168.
25. Reyes JC, Muchardt C, Yaniv M. 1997. Components of the human SWI/SNF complex are enriched in active chromatin and are associated with the nuclear matrix. J Cell Biol 137:263-274.
26. Romanato M, Cameo MS, Bertolesi G, Baldini C, Calvo JC, Calvo L. 2003. Heparan sulphate: A putative decondensing agent for human spermatozoa in vivo. Hum Reprod 18:1868-1873.
27. Romanato M, Regueira E, Cameo MS, Baldini C, Calvo L, Calvo JC. 2005. Further evidence on the role of heparan sulfate as protamine acceptor during the decondensation of human spermatozoa. Hum Reprod 20:2784-2789.
28. Romanato M, Julianelli V, Zappi M, Calvo L, Calvo JC. 2008. The presence of heparan sulfate in the mammalian oocyte provides a clue to human sperm nuclear decondensation in vivo. Hum Reprod 23:1145-1150.
29. Schneider M, Forster H, Boersma A, Seiler A, Wehnes H, Sinowatz F, Neumuller C, Deutsch MJ, Walch A, Hrabe DA, Wurst W, Ursini F, Roveri A, Maleszewski M, Maiorino M, Conrad M. 2009. Mitochondrial glutathione peroxidase 4 disruption causes male infertility. FASEB J 23:3233-3242.
30. Shaman JA, Yamauchi Y, Ward WS. 2007. The sperm nuclear matrix is required for paternal DNA replication. J Cell Biochem 102:680-688.
31. Sutovsky P, Schatten G. 1997. Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol Reprod 56:1503-1512.
32. Tang CW, Maya-Mendoza A, Martin C, Zeng K, Chen S, Feret D, Wilson SA, Jackson DA. 2008. The integrity of a lamin-B1-dependent nucleoskeleton is a fundamental determinant of RNA synthesis in human cells. J Cell Sci 121:1014-1024.
33. Tatone C, Van Eekelen CG, Colonna R. 1994. Plasma membrane block to sperm entry occurs in mouse eggs upon parthenogenetic activation. Mol Reprod Dev 38:200-208.
34. Tramer F, Micali F, Sandri G, Bertoni A, Lenzi A, Gandini L, Panfili E. 2002. Enzymatic and immunochemical evaluation of phospholipid hydroperoxide glutathione peroxidase (PHGPx) in testes and epididymal spermatozoa of rats of different ages. Int J Androl 25:72-83.
35. 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.
36. van der Heijden GW, Dieker JW, Derijck AA, Muller S, Berden JH, Braat DD, van d V, de Boer P. 2005. Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech Dev 122:1008-1022.
37. Ward WS. 2010. Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod 16:30-36.
38. Ward WS, Kimura Y, Yanagimachi R. 1999. An intact sperm nuclear matrix may be necessary for the mouse paternal genome to participate in embryonic development. Biol Reprod 60:702-706.
39. Watanabe T, Endo A. 1991. Effects of selenium deficiency on sperm morphology and spermatocyte chromosomes in mice. Mutat Res 262:93-99.
40. Wu JY, Ribar TJ, Cummings DE, Burton KA, McKnight GS, Means AR. 2000. Spermiogenesis and exchange of basic nuclear proteins are impaired in male germ cells lacking Camk4. Nat Genet 25:448-452.
41. Yamauchi Y, Shaman JA, Boaz SM, Ward WS. 2007. Paternal pronuclear DNA degradation is functionally linked to DNA replication in mouse oocytes. Biol Reprod 77:407-415.
42. Zeng C, van Wijnen AJ, Stein JL, Meyers S, Sun W, Shopland L, Lawrence JB, Penman S, Lian JB, Stein GS, Hiebert SW. 1997. Identification of a nuclear matrix targeting signal in the leukemia and bone-related AML/CBF-alpha transcription factors. Proc Natl Acad Sci USA 94:6746-6751.