Ubiquitination of prohibitin in mammalian sperm mitochondria: Possible roles in the regulation of mitochondrial inheritance and sperm quality control

Biology of Reproduction

Volumn 69, Issue 1, 2003, Pages 254-260

  Thompson, Winston E ^a   Ramalho Santos, João ^b   Sutovsky, Peter ^c  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

Epididymis; Fertilization; Gamete biology; Sperm maturation; Spermatogenesis

Indexed keywords

ANTIBODY; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MITOCHONDRIAL DNA; PROHIBITIN; PROHIBITIN ANTIBODY; TUBULIN; UBIQUITIN ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; AXONEME; CATTLE; CONTROLLED STUDY; DNA BINDING; EJACULATION; EPIDIDYMIS; EXTRACHROMOSOMAL INHERITANCE; FERTILIZATION; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; MALE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; PRECIPITATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN MODIFICATION; QUALITY CONTROL; SPERM; SPERMATID; SPERMATOGENESIS; SPERMATOZOON ABNORMALITY; UBIQUITINATION; WESTERN BLOTTING;

ANIMALS; CATTLE; EPIDIDYMIS; FEMALE; FERTILIZATION; HUMANS; MALE; MICROSCOPY, IMMUNOELECTRON; MITOCHONDRIA; PROTEINS; REPRESSOR PROTEINS; SPERMATOGENESIS; SPERMATOZOA; UBIQUITIN;

ANIMALIA; BOS TAURUS; MAMMALIA;

EID: 0037774827     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.102.010975     Document Type: Article

References (40)

1. Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G. Ubiquitin tag for sperm mitochondria. Nature 1999; 402:371-372.
2. Sutovsky P, Moreno R, Ramalho-Santos J, Dominko T, Simerly C, Schatten G. Ubiquitinated sperm mitochondria, selective proteolysis and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod 2000; 63:582-590.
3. Ingman M, Kaessmann H, Paabo S, Gyllensten U. Mitochondrial genome variation and the origin of modern humans. Nature 2000; 408:708-713.
4. Kaneda H, Hayashi J-I, Takahama S, Taya C, Fischer-Lindahl K, Yonekawa H. Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci U S A 1995; 92:4542-4546.
5. Shitara H, Kaneda H, Sato A, Inoue K, Ogura A, Yonekawa H, Hayashi JI. Selective and continuous elimination of mitochondria micro-injected into mouse eggs from spermatids, but not from liver cells, occurs throughout embryogenesis. Genetics 2000; 156:1277-1284.
6. Schwartz M, Vissing J. Paternal inheritance of mitochondrial DNA. N Engl J Med 2002; 22:576-580.
7. Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998; 67:425-479.
8. Conaway RC, Brower CS, Conaway JW. Emerging roles of ubiquitin in transcription regulation. Science 2002; 296:1254-1258.
9. Chen HY, Sun JM, Zhang Y, Davie JR, Meistrich ML. Ubiquitination of histone H3 in elongating spermatids of rat testes. J Biol Chem 1998; 273:13165-13269.
10. Baarends WM, Hoogerbrugge JW, Roest HP, Ooms M, Vreeburg J, Hoeijmakers JH, Grootegoed JA. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev Biol 1999; 207:322-333.
11. Rajapurohitam V, Morales CR, El-Alfy M, Lefrancois S, Bedard N, Wing SS. Activation of a UBC4-dependent pathway of ubiquitin conjugation during postnatal development of the rat testis. Dev Biol 1999; 212:217-228.
12. Wing SS, Bedard N, Morales C, Hingamp P, Trasler J. A novel rat homolog of the Saccharomyces cerevisiae ubiquitin-conjugating enzymes UBC4 and UBC5 with distinct biochemical features is induced during spermatogenesis. Mol Cell Biol 1996; 16:4064-4072.
13. Fraile B, Martin R, De Miguel MP, Arenas MI, Bethencourt FR, Peinado F, Paniagua R, Santamaria L. Light and electron microscopic immunohistochemical localization of protein gene product 9.5 and ubiquitin immunoreactivities in the human epididymis and vas deferens. Biol Reprod 1996; 55:291-297.
14. Sutovsky P, Moreno R, Ramalho-Santos J, Dominko T, Thompson WE, Schatten G. A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J Cell Sci 2001; 114:1665-1675.
15. Lippert TH, Seeger H, Schieferstein G, Voelter W. Immunoreactive ubiquitin in human seminal plasma. J Androl 1993; 14:130-131.
16. Sutovsky P, Terada Y, Schatten G. Ubiquitin-based sperm assay for the diagnosis of male factor infertility. Hum Reprod 2001; 16:250-258.
17. Rawe VY, Brugo Olmedo S, Benmusa A, Shiigi SM, Chemes HE, Sutovsky P. Sperm Ubiquitination in Patients with Dysplasia of the Fibrous Sheath. Hum Reprod 2002; 17:2119-2127.
18. Arnold I, Langer T. Membrane protein degradation by AAA proteases in mitochondria. Biochim Biophys Acta 2002; 1592:89-96.
19. Choongkittaworn NM, Kim KH, Danner DB, Griswold MD. Expression of prohibitin in rat seminiferous epithelium. Biol Reprod 1993; 49:300-310.
20. McClung JK, Danner DB, Stewart DA, Smith JR, Schneider EL, Lumpkin CK, Dell'Orco RT, Nuell MJ. Isolation of a cDNA that hybrid selects antiproliferative mRNA from rat liver. Biochem Biophys Res Commun 1989; 164:1316-1322.
21. Nuell MJ, Stewart DA, Walker L, Friedman V, Wood CM, Owen GA, Smith JR, Schneider EL, Dell'Orco R, Lumpkin CK. Prohibitin, an evolutionarily conserved intracellular protein that blocks DNA synthesis in normal fibroblasts and HeLa cells. Mol Cell Biol 1991; 11:1372-1381.
22. McClung JK, Jupe ER, Liu XT, Dell'Orco RT. Prohibitin: potential role in senescence, development, and tumor suppression. Exp Gerontol 1995; 30:99-124.
23. Roskams AJ, Friedman V, Wood CM, Walker L, Owens GA, Stewart DA, Altus MS, Danner DB, Liu XT, McClung JK. Cell cycle activity and expression of prohibitin mRNA. J Cell Physiol 1993; 157:289-295.
24. Thompson WE, Sanbuissho A, Lee GY, Anderson E. Steroidogenic acute regulatory (StAR) protein (p25) and prohibitin (p28) from cultured rat ovarian granulosa cells. J Reprod Fertil 1997; 109:337-348.
25. Thompson WE, Powell JM, Whittaker JA, Sridaran R, Thomas KH. Immunolocalization and expression of prohibitin, a mitochondrial associated protein within the rat ovaries. Anat Rec 1999; 256:40-48.
26. Thompson WE, Branch A, Whittaker JA, Lyn D, Zilberstein M, Mayo KE, Thomas K. Characterization of prohibitin in a newly established rat ovarian granulosa cell line. Endocrinology 2001; 142:4076-4085.
27. Jupe ER, Liu XT, Kiehlbauch JL, McClung JK, Dell'Orco RT. Prohibitin antiproliferative activity and lack of heterozygosity in immortalized cell lines. Exp Cell Res 1995; 218:577-580.
28. Jupe ER, Liu XT, Kiehlbauch JL, McClung JK, Dell'Orco RT. The 3′ untranslated region of prohibitin and cellular immortalization. Exp Cell Res 1996; 224:128-135.
29. Sutovsky P, Neuber E, Schatten G. Ubiquitin-dependent, sperm quality control mechanism recognizes spermatozoa with DNA defects, as revealed by dual ubiquitin-TUNEL assay. Mol Reprod Dev 2002; 61:406-413.
30. Pickart CM. Polyubiquitin chains. In: Peters J-M, Harris JR, Finley D (eds.), Ubiquitin and the Biology of the Cell. New York: Plenum Press; 1998:19-63.
31. Sutovsky P, McCauley TC, Sutovsky M, Day BN. Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG 132. Biol Reprod 2002; 68:1793-1800.
32. Miranda-Vizuete A, Ljung J, Damdimopoulos AE, Gustafsson JA, Oko R, Pelto-Huikko M, Spyrou G. Characterization of Sptrx, a novel member of the thioredoxin family specifically expressed in human spermatozoa. J Biol Chem 2001; 276:31567-31574.
33. Perreault SD, Wolff RA, Zirkin BR. The role of disulfide bond reduction during mammalian sperm nuclear decondensation in vivo. Dev Biol 1984; 101:160-167.
34. Sutovsky P, Schatten G. Depletion of glutathione during oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol Reprod 1997; 56:1503-1512.
35. Jurisicova A, Latham KE, Casper RF, Casper RF, Varmuza SL. Expression and regulation of genes associated with cell death during murine preimplantation embryo development. Mol Reprod Dev 1998; 51:243-253.
36. Jesenberger V, Jentsch S. Deadly encounter: ubiquitin meets apoptosis. Nat Rev Mol Cell Biol 2002; 3:112-121.
37. Fisk HA, Yaffe MP. A role for ubiquitination in mitochondrial inheritance in Saccharomyces cerevisiae. J Cell Biol 1999; 145:1199-1208.
38. Berger KH, Yaffe MP. Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae. Mol Cell Biol 1998; 18:4043-4052.
39. Sutovsky P. Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: killing three birds with one stone. Microsc Res Tech 2003; 61:88-102.
40. Hiendleder S, Schmutz SM, Erhardt G, Green RD, Plante Y. Transmitochondrial differences and varying levels of heteroplasmy in nuclear transfer cloned cattle. Mol Reprod Dev 1999; 54:24-31.