Skip to main content

Deubiquitinating Enzymes in Oocyte Maturation, Fertilization and Preimplantation Embryo Development

  • Chapter
  • First Online:

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 759))

Abstract

Post-translational modifications of cellular proteins by ubiquitin and ubiquitin-like protein modifiers are important regulatory events involved in diverse aspects of gamete and embryo physiology including oocyte maturation, fertilization and development of embryos to term. Deubiquitinating enzymes (DUBs) regulate proteolysis by reversing ubiquitination, which targets proteins to the 26S proteasome. The ubiquitin C-terminal hydrolases (UCHs) comprise are DUBs that play a role in the removal of multi-ubiquitin chains. We review here the roles of UCHs in oocytes maturation, fertilization and development in mouse, bovine, porcine and rhesus monkeys. Oocyte UCHs contributes to fertilization and embryogenesis by regulating the physiology of the oocyte and blastomere cortex as well as oocyte spindle. Lack of UCHs in embryos reduces fertilization, while mutant embryos fail to undergo compaction and blastocyst formation. In addition to advancing our understanding of reproductive process, research on the role of deubiquitinating enzymes will allow us to better understand and treat human infertility, and to optimize reproductive performance in agriculturally important livestock species.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  1. Consortium IHGS. Finishing the euchromatic sequence of the human genome. Nature. 2004;431(7011):931–45.

    Google Scholar 

  2. Jensen ON. Modification-specific proteomics: characterization of post-translational modifications by mass spectrometry. Curr Opin Chem Biol. 2004;8(1):33–41.

    PubMed  Google Scholar 

  3. Ayoubi TA, Van De Ven WJ. Regulation of gene expression by alternative promoters. FASEB J. 1996;10(4):453–60.

    CAS  PubMed  Google Scholar 

  4. Walsh C. Posttranslational modification of proteins: expanding nature’s inventory. Englewood, CO: Roberts; 2005.

    Google Scholar 

  5. Glickman MH, Ciechanover A. The ubiquitin–proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev. 2002;82(2):373–428.

    CAS  PubMed  Google Scholar 

  6. Dice JF. Peptide sequences that target cytosolic proteins for lysosomal proteolysis. Trends Biochem Sci. 1990;15(8):305–9.

    CAS  PubMed  Google Scholar 

  7. Dice JF, Terlecky SR, Chiang HL, Olson TS, Isenman LD, Short-Russell SR, et al. A selective pathway for degradation of cytosolic proteins by lysosomes. Semin Cell Biol. 1990;1(6):449–55.

    CAS  PubMed  Google Scholar 

  8. Turk V, Turk B, Turk D. Lysosomal cysteine proteases: facts and opportunities. EMBO J. 2001;20(17):4629–33.

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Turk B, Turk D, Turk V. Lysosomal cysteine proteases: more than scavengers. Biochim Biophys Acta. 2000;1477(1–2):98–111.

    CAS  PubMed  Google Scholar 

  10. Lysosomal proteases: revival of the sleeping beauty. ***[database on the Internet]. Landes Bioscience, Austin, TX. 2000 [cited].

    Google Scholar 

  11. Kirkin V, McEwan DG, Novak I, Dikic I. A role for ubiquitin in selective autophagy. Mol Cell. 2009;34(3):259–69.

    CAS  PubMed  Google Scholar 

  12. Ciehanover A, Hod Y, Hershko A. A heat-stable polypeptide component of an ATP-dependent proteolytic system from reticulocytes. Biochem Biophys Res Commun. 1978;81(4):1100–5.

    CAS  PubMed  Google Scholar 

  13. Nakayama KI, Nakayama K. Ubiquitin ligases: cell-cycle control and cancer. Nat Rev Cancer. 2006;6(5):369–81.

    CAS  PubMed  Google Scholar 

  14. Ciechanover A. Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin–proteasome system and onto human diseases and drug targeting. Bioorg Med Chem. 2013;21(12):3400–10.

    CAS  PubMed  Google Scholar 

  15. Bassermann F, Eichner R, Pagano M. The ubiquitin proteasome system—implications for cell cycle control and the targeted treatment of cancer. Biochim Biophys Acta. 2014;1843(1): 150–62.

    CAS  PubMed  Google Scholar 

  16. Wilkinson KD. DUBs at a glance. J Cell Sci. 2009;122(Pt 14):2325–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Weissman AM. Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol. 2001;2(3):169–78.

    CAS  PubMed  Google Scholar 

  18. Hoppe T. Multiubiquitylation by E4 enzymes: ‘one size’ doesn’t fit all. Trends Biochem Sci. 2005;30(4):183–7.

    CAS  PubMed  Google Scholar 

  19. Zhang Y. Transcriptional regulation by histone ubiquitination and deubiquitination. Genes Dev. 2003;17(22):2733–40.

    CAS  PubMed  Google Scholar 

  20. Hershko A, Heller H, Elias S, Ciechanover A. Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J Biol Chem. 1983;258(13):8206–14.

    CAS  PubMed  Google Scholar 

  21. Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem. 1998;67:425–79.

    CAS  PubMed  Google Scholar 

  22. Bachmair A, Finley D, Varshavsky A. In vivo half-life of a protein is a function of its amino-terminal residue. Science. 1986;234(4773):179–86.

    CAS  PubMed  Google Scholar 

  23. Bachmair A, Varshavsky A. The degradation signal in a short-lived protein. Cell. 1989;56(6):1019–32.

    CAS  PubMed  Google Scholar 

  24. Gonda DK, Bachmair A, Wunning I, Tobias JW, Lane WS, Varshavsky A. Universality and structure of the N-end rule. J Biol Chem. 1989;264(28):16700–12.

    CAS  PubMed  Google Scholar 

  25. Sutovsky P. Sperm proteasome and fertilization. Reproduction. 2011;142(1):1–14.

    CAS  PubMed  Google Scholar 

  26. Komander D, Clague MJ, Urbe S. Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol. 2009;10(8):550–63.

    CAS  PubMed  Google Scholar 

  27. Amerik AY, Hochstrasser M. Mechanism and function of deubiquitinating enzymes. Biochim Biophys Acta. 2004;1695(1–3):189–207.

    CAS  PubMed  Google Scholar 

  28. D’Andrea A, Pellman D. Deubiquitinating enzymes: a new class of biological regulators. Crit Rev Biochem Mol Biol. 1998;33(5):337–52.

    PubMed  Google Scholar 

  29. Komander D. Mechanism, specificity and structure of the deubiquitinases. Subcell Biochem. 2011;54:69–87.

    Google Scholar 

  30. Shanmugham A, Ovaa H. DUBs and disease: activity assays for inhibitor development. Curr Opin Drug Discov Devel. 2008;11(5):688–96.

    CAS  PubMed  Google Scholar 

  31. Singhal S, Taylor MC, Baker RT. Deubiquitylating enzymes and disease. BMC Biochem. 2008;9 Suppl 1:S3.

    PubMed Central  PubMed  Google Scholar 

  32. Setsuie R, Wada K. The functions of UCH-L1 and its relation to neurodegenerative diseases. Neurochem Int. 2007;51(2–4):105–11.

    CAS  PubMed  Google Scholar 

  33. Zhu P, Zhou W, Wang J, Puc J, Ohgi KA, Erdjument-Bromage H, et al. A histone H2A deubiquitinase complex coordinating histone acetylation and H1 dissociation in transcriptional regulation. Mol Cell. 2007;27(4):609–21.

    CAS  PubMed Central  PubMed  Google Scholar 

  34. Larsen CN, Krantz BA, Wilkinson KD. Substrate specificity of deubiquitinating enzymes: ubiquitin C-terminal hydrolases. Biochemistry. 1998;37(10):3358–68.

    CAS  PubMed  Google Scholar 

  35. Wilkinson KD, Tashayev VL, O’Connor LB, Larsen CN, Kasperek E, Pickart CM. Metabolism of the polyubiquitin degradation signal: structure, mechanism, and role of isopeptidase T. Biochemistry. 1995;34(44):14535–46.

    CAS  PubMed  Google Scholar 

  36. Dayal S, Sparks A, Jacob J, Allende-Vega N, Lane DP, Saville MK. Suppression of the deubiquitinating enzyme USP5 causes the accumulation of unanchored polyubiquitin and the activation of p53. J Biol Chem. 2009;284(8):5030–41.

    CAS  PubMed Central  PubMed  Google Scholar 

  37. Butterworth MB, Edinger RS, Ovaa H, Burg D, Johnson JP, Frizzell RA. The deubiquitinating enzyme UCH-L3 regulates the apical membrane recycling of the epithelial sodium channel. J Biol Chem. 2007;282(52):37885–93.

    CAS  PubMed  Google Scholar 

  38. Machida YJ, Machida Y, Vashisht AA, Wohlschlegel JA, Dutta A. The deubiquitinating enzyme BAP1 regulates cell growth via interaction with HCF-1. J Biol Chem. 2009;284(49):34179–88.

    CAS  PubMed Central  PubMed  Google Scholar 

  39. Misaghi S, Ottosen S, Izrael-Tomasevic A, Arnott D, Lamkanfi M, Lee J, et al. Association of C-terminal ubiquitin hydrolase BRCA1-associated protein 1 with cell cycle regulator host cell factor 1. Mol Cell Biol. 2009;29(8):2181–92.

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Nakagawa T, Kajitani T, Togo S, Masuko N, Ohdan H, Hishikawa Y, et al. Deubiquitylation of histone H2A activates transcriptional initiation via trans-histone cross-talk with H3K4 di- and trimethylation. Genes Dev. 2008;22(1):37–49.

    CAS  PubMed Central  PubMed  Google Scholar 

  41. Winborn BJ, Travis SM, Todi SV, Scaglione KM, Xu P, Williams AJ, et al. The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J Biol Chem. 2008;283(39):26436–43.

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Lam YA, Xu W, DeMartino GN, Cohen RE. Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature. 1997;385(6618):737–40.

    CAS  PubMed  Google Scholar 

  43. McCullough J, Clague MJ, Urbe S. AMSH is an endosome-associated ubiquitin isopeptidase. J Cell Biol. 2004;166(4):487–92.

    CAS  PubMed Central  PubMed  Google Scholar 

  44. McCullough J, Row PE, Lorenzo O, Doherty M, Beynon R, Clague MJ, et al. Activation of the endosome-associated ubiquitin isopeptidase AMSH by STAM, a component of the multivesicular body-sorting machinery. Curr Biol. 2006;16(2):160–5.

    CAS  PubMed  Google Scholar 

  45. Kim JH, Park KC, Chung SS, Bang O, Chung CH. Deubiquitinating enzymes as cellular regulators. J Biochem. 2003;134(1):9–18.

    CAS  PubMed  Google Scholar 

  46. Fang Y, Fu D, Shen XZ. The potential role of ubiquitin c-terminal hydrolases in oncogenesis. Biochim Biophys Acta. 2010;1806(1):1–6.

    CAS  PubMed  Google Scholar 

  47. Wilkinson KD, Lee KM, Deshpande S, Duerksen-Hughes P, Boss JM, Pohl J. The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science. 1989;246(4930): 670–3.

    CAS  PubMed  Google Scholar 

  48. Osaka H, Wang YL, Takada K, Takizawa S, Setsuie R, Li H, et al. Ubiquitin carboxy-terminal hydrolase L1 binds to and stabilizes monoubiquitin in neuron. Hum Mol Genet. 2003;12(16):1945–58.

    CAS  PubMed  Google Scholar 

  49. Ellederova Z, Halada P, Man P, Kubelka M, Motlik J, Kovarova H. Protein patterns of pig oocytes during in vitro maturation. Biol Reprod. 2004;71(5):1533–9.

    CAS  PubMed  Google Scholar 

  50. Massicotte L, Coenen K, Mourot M, Sirard MA. Maternal housekeeping proteins translated during bovine oocyte maturation and early embryo development. Proteomics. 2006;6(13): 3811–20.

    CAS  PubMed  Google Scholar 

  51. Larsen K, Madsen LB, Bendixen C. Porcine UCHL1: genomic organization, chromosome localization and expression analysis. Mol Biol Rep. 2012;39(2):1095–103.

    CAS  PubMed  Google Scholar 

  52. Jackson P, Thompson RJ. The demonstration of new human brain-specific proteins by high-resolution two-dimensional polyacrylamide gel electrophoresis. J Neurol Sci. 1981; 49(3): 429–38.

    CAS  PubMed  Google Scholar 

  53. Johnston SC, Larsen CN, Cook WJ, Wilkinson KD, Hill CP. Crystal structure of a deubiquitinating enzyme (human UCH-L3) at 1.8 A resolution. EMBO J. 1997;16(13):3787–96.

    CAS  PubMed Central  PubMed  Google Scholar 

  54. Mtango NR, Sutovsky M, Susor A, Zhong Z, Latham KE, Sutovsky P. Essential role of maternal UCHL1 and UCHL3 in fertilization and preimplantation embryo development. J Cell Physiol. 2012;227(4):1592–603.

    CAS  PubMed  Google Scholar 

  55. Susor A, Liskova L, Toralova T, Pavlok A, Pivonkova K, Karabinova P, et al. Role of ubiquitin C-terminal hydrolase-L1 in antipolyspermy defense of mammalian oocytes. Biol Reprod. 2010;82(6):1151–61.

    CAS  PubMed  Google Scholar 

  56. Yi YJ, Manandhar G, Sutovsky M, Li R, Jonakova V, Oko R, et al. Ubiquitin C-terminal hydrolase-activity is involved in sperm acrosomal function and anti-polyspermy defense during porcine fertilization. Biol Reprod. 2007;77(5):780–93.

    CAS  PubMed  Google Scholar 

  57. Sekiguchi S, Kwon J, Yoshida E, Hamasaki H, Ichinose S, Hideshima M, et al. Localization of ubiquitin C-terminal hydrolase L1 in mouse ova and its function in the plasma membrane to block polyspermy. Am J Pathol. 2006;169(5):1722–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Liu Y, Fallon L, Lashuel HA, Liu Z, Lansbury Jr PT. The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson’s disease susceptibility. Cell. 2002;111(2):209–18.

    CAS  PubMed  Google Scholar 

  59. Li R, Albertini DF. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol. 2013;14(3):141–52.

    CAS  PubMed  Google Scholar 

  60. Mtango NR, Potireddy S, Latham KE. Oocyte quality and maternal control of development. Int Rev Cell Mol Biol. 2008;268:223–90.

    CAS  PubMed  Google Scholar 

  61. Dekel N. Cellular, biochemical and molecular mechanisms regulating oocyte maturation. Mol Cell Endocrinol. 2005;234(1–2):19–25.

    CAS  PubMed  Google Scholar 

  62. Josefsberg LB, Galiani D, Dantes A, Amsterdam A, Dekel N. The proteasome is involved in the first metaphase-to-anaphase transition of meiosis in rat oocytes. Biol Reprod. 2000;62(5): 1270–7.

    CAS  PubMed  Google Scholar 

  63. Mtango NR, Sutovsky M, Vandevoort CA, Latham KE, Sutovsky P. Essential role of ubiquitin C-terminal hydrolases UCHL1 and UCHL3 in mammalian oocyte maturation. J Cell Physiol. 2012;227(5):2022–9.

    CAS  PubMed  Google Scholar 

  64. Susor A, Ellederova Z, Jelinkova L, Halada P, Kavan D, Kubelka M, et al. Proteomic analysis of porcine oocytes during in vitro maturation reveals essential role for the ubiquitin C-terminal hydrolase-L1. Reproduction. 2007;134(4):559–68.

    CAS  PubMed  Google Scholar 

  65. Koyanagi S, Hamasaki H, Sekiguchi S, Hara K, Ishii Y, Kyuwa S, et al. Effects of ubiquitin C-terminal hydrolase L1 deficiency on mouse ova. Reproduction. 2012;143(3):271–9.

    CAS  PubMed  Google Scholar 

  66. Yi YJ, Nagyova E, Manandhar G, Prochazka R, Sutovsky M, Park CS, et al. Proteolytic activity of the 26S proteasome is required for the meiotic resumption, germinal vesicle breakdown, and cumulus expansion of porcine cumulus–oocyte complexes matured in vitro. Biol Reprod. 2008;78(1):115–26.

    CAS  PubMed  Google Scholar 

  67. Nagyova E, Scsukova S, Nemcova L, Mlynarcikova A, Yi YJ, Sutovsky M, et al. Inhibition of proteasomal proteolysis affects expression of extracellular matrix components and steroidogenesis in porcine oocyte–cumulus complexes. Domest Anim Endocrinol. 2011;42(1): 50–62.

    PubMed  Google Scholar 

  68. Maro B, Johnson MH, Webb M, Flach G. Mechanism of polar body formation in the mouse oocyte: an interaction between the chromosomes, the cytoskeleton and the plasma membrane. J Embryol Exp Morphol. 1986;92:11–32.

    CAS  PubMed  Google Scholar 

  69. Verlhac MH, Lefebvre C, Guillaud P, Rassinier P, Maro B. Asymmetric division in mouse oocytes: with or without Mos. Curr Biol. 2000;10(20):1303–6.

    CAS  PubMed  Google Scholar 

  70. Azoury J, Lee KW, Georget V, Rassinier P, Leader B, Verlhac MH. Spindle positioning in mouse oocytes relies on a dynamic meshwork of actin filaments. Curr Biol. 2008;18(19):1514–9.

    CAS  PubMed  Google Scholar 

  71. Brugues J, Nuzzo V, Mazur E, Needleman DJ. Nucleation and transport organize microtubules in metaphase spindles. Cell. 2012;149(3):554–64.

    CAS  PubMed  Google Scholar 

  72. Schuh M, Ellenberg J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell. 2007;130(3):484–98.

    CAS  PubMed  Google Scholar 

  73. Xu XL, Ma W, Zhu YB, Wang C, Wang BY, An N, et al. The microtubule-associated protein ASPM regulates spindle assembly and meiotic progression in mouse oocytes. PLoS One. 2012;7(11):e49303.

    CAS  PubMed Central  PubMed  Google Scholar 

  74. Azoury J, Verlhac MH, Dumont J. Actin filaments: key players in the control of asymmetric divisions in mouse oocytes. Biol Cell. 2009;101(2):69–76.

    CAS  PubMed  Google Scholar 

  75. Schuh M, Ellenberg J. A new model for asymmetric spindle positioning in mouse oocytes. Curr Biol. 2008;18(24):1986–92.

    CAS  PubMed  Google Scholar 

  76. Azoury J, Lee KW, Georget V, Hikal P, Verlhac MH. Symmetry breaking in mouse oocytes requires transient F-actin meshwork destabilization. Development. 2011;138(14):2903–8.

    CAS  PubMed  Google Scholar 

  77. Wang S, Hu J, Guo X, Liu JX, Gao S. ADP-ribosylation factor 1 regulates asymmetric cell division in female meiosis in the mouse. Biol Reprod. 2009;80(3):555–62.

    CAS  PubMed  Google Scholar 

  78. Cinnamon Y, Feine O, Hochegger H, Bershadsky A, Brandeis M. Cellular contractility requires ubiquitin mediated proteolysis. PLoS One. 2009;4(7):e6155.

    PubMed Central  PubMed  Google Scholar 

  79. DeWard AD, Alberts AS. Ubiquitin-mediated degradation of the formin mDia2 upon completion of cell division. J Biol Chem. 2009;284(30):20061–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Keller JN, Markesbery WR. Proteasome inhibition results in increased poly-ADP-ribosylation: implications for neuron death. J Neurosci Res. 2000;61(4):436–42.

    CAS  PubMed  Google Scholar 

  81. Lee FJ, Moss J, Vaughan M. Human and Giardia ADP-ribosylation factors (ARFs) complement ARF function in Saccharomyces cerevisiae. J Biol Chem. 1992;267(34):24441–5.

    CAS  PubMed  Google Scholar 

  82. Yano H, Kobayashi I, Onodera Y, Luton F, Franco M, Mazaki Y, et al. Fbx8 makes Arf6 refractory to function via ubiquitination. Mol Biol Cell. 2008;19(3):822–32.

    CAS  PubMed Central  PubMed  Google Scholar 

  83. Kaitna S, Schnabel H, Schnabel R, Hyman AA, Glotzer M. A ubiquitin C-terminal hydrolase is required to maintain osmotic balance and execute actin-dependent processes in the early C. elegans embryo. J Cell Sci. 2002;115(Pt 11):2293–302.

    CAS  PubMed  Google Scholar 

  84. Pomerantz Y, Elbaz J, Ben-Eliezer I, Reizel Y, David Y, Galiani D, et al. From ubiquitin-proteasomal degradation to CDK1 inactivation: requirements for the first polar body extrusion in mouse oocytes. FASEB J. 2012;26(11):4495–505.

    CAS  PubMed  Google Scholar 

  85. Munne S, Alikani M, Tomkin G, Grifo J, Cohen J. Embryo morphology, developmental rates, and maternal age are correlated with chromosome abnormalities. Fertil Steril. 1995;64(2): 382–91.

    CAS  PubMed  Google Scholar 

  86. Munne S, Chen S, Colls P, Garrisi J, Zheng X, Cekleniak N, et al. Maternal age, morphology, development and chromosome abnormalities in over 6000 cleavage-stage embryos. Reprod Biomed Online. 2007;14(5):628–34.

    CAS  PubMed  Google Scholar 

  87. Bielanska M, Tan SL, Ao A. Chromosomal mosaicism throughout human preimplantation development in vitro: incidence, type, and relevance to embryo outcome. Hum Reprod. 2002;17(2):413–9.

    PubMed  Google Scholar 

  88. Magli MC, Gianaroli L, Ferraretti AP, Lappi M, Ruberti A, Farfalli V. Embryo morphology and development are dependent on the chromosomal complement. Fertil Steril. 2007;87(3):534–41.

    PubMed  Google Scholar 

  89. Henderson SA, Edwards RG. Chiasma frequency and maternal age in mammals. Nature. 1968;218(5136):22–8.

    CAS  PubMed  Google Scholar 

  90. Hassold T, Chiu D. Maternal age-specific rates of numerical chromosome abnormalities with special reference to trisomy. Hum Genet. 1985;70(1):11–7.

    CAS  PubMed  Google Scholar 

  91. Battaglia DE, Goodwin P, Klein NA, Soules MR. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod. 1996;11(10):2217–22.

    CAS  PubMed  Google Scholar 

  92. Hunt PA, Hassold TJ. Human female meiosis: what makes a good egg go bad? Trends Genet. 2008;24(2):86–93.

    CAS  PubMed  Google Scholar 

  93. Selesniemi K, Lee HJ, Muhlhauser A, Tilly JL. Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies. Proc Natl Acad Sci U S A. 2011;108(30):12319–24.

    CAS  PubMed Central  PubMed  Google Scholar 

  94. Goshima G, Wollman R, Stuurman N, Scholey JM, Vale RD. Length control of the metaphase spindle. Curr Biol. 2005;15(22):1979–88.

    CAS  PubMed  Google Scholar 

  95. Shao H, Ma C, Zhang X, Li R, Miller AL, Bement WM, et al. Aurora B regulates spindle bipolarity in meiosis in vertebrate oocytes. Cell Cycle. 2012;11(14):2672–80.

    CAS  PubMed Central  PubMed  Google Scholar 

  96. Ueno S, Kurome M, Ueda H, Tomii R, Hiruma K, Nagashima H. Effects of maturation conditions on spindle morphology in porcine MII oocytes. J Reprod Dev. 2005;51(3):405–10.

    PubMed  Google Scholar 

  97. Doubilet S, McKim KS. Spindle assembly in the oocytes of mouse and Drosophila–similar solutions to a problem. Chromosome Res. 2007;15(5):681–96.

    CAS  PubMed  Google Scholar 

  98. Guo X, Gao S. Pins homolog LGN regulates meiotic spindle organization in mouse oocytes. Cell Res. 2009;19(7):838–48.

    CAS  PubMed  Google Scholar 

  99. Schatten H, Sun QY. The functional significance of centrosomes in mammalian meiosis, fertilization, development, nuclear transfer, and stem cell differentiation. Environ Mol Mutagen. 2009;50(8):620–36.

    CAS  PubMed  Google Scholar 

  100. Huo LJ, Zhong ZS, Liang CG, Wang Q, Yin S, Ai JS, et al. Degradation of securin in mouse and pig oocytes is dependent on ubiquitin–proteasome pathway and is required for proteolysis of the cohesion subunit, Rec8, at the metaphase-to-anaphase transition. Front Biosci. 2006;11:2193–202.

    CAS  PubMed  Google Scholar 

  101. Yanagida M. Basic mechanism of eukaryotic chromosome segregation. Philos Trans R Soc Lond B Biol Sci. 2005;360(1455):609–21.

    CAS  PubMed Central  PubMed  Google Scholar 

  102. Kurz T, Pintard L, Willis JH, Hamill DR, Gonczy P, Peter M, et al. Cytoskeletal regulation by the Nedd8 ubiquitin-like protein modification pathway. Science. 2002;295(5558):1294–8.

    CAS  PubMed  Google Scholar 

  103. Sawada H, Sakai N, Abe Y, Tanaka E, Takahashi Y, Fujino J, et al. Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor. Proc Natl Acad Sci U S A. 2002;99(3):1223–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  104. Yokota N, Sawada H. Effects of proteasome inhibitors on fertilization of the sea urchin Anthocidaris crassispina. Biol Pharm Bull. 2007;30(7):1332–5.

    CAS  PubMed  Google Scholar 

  105. Mtango NR, Sutovsky M, Susor A, Zhong Z, Latham KE, Sutovsky P. Essential role of maternal UCHL1 and UCHL3 in fertilization and preimplantation embryo development. J Cell Physiol. 2012;227(4):1592–603.

    CAS  PubMed  Google Scholar 

  106. Wang H, Song C, Duan C, Shi W, Li C, Chen D, et al. Effects of ubiquitin proteasome pathway on mouse sperm capacitation, acrosome reaction and in vitro fertilization. Chin Sci Bull. 2002;47:127–32.

    CAS  Google Scholar 

  107. Mtango NR, Latham KE. Ubiquitin proteasome pathway gene expression varies in rhesus monkey oocytes and embryos of different developmental potential. Physiol Genomics. 2007;31(1):1–14.

    CAS  PubMed  Google Scholar 

  108. Rawe VY, Diaz ES, Abdelmassih R, Wojcik C, Morales P, Sutovsky P, et al. The role of sperm proteasomes during sperm aster formation and early zygote development: implications for fertilization failure in humans. Hum Reprod. 2008;23(3):573–80.

    CAS  PubMed  Google Scholar 

  109. Plachot M, Mandelbaum J. Oocyte maturation, fertilization and embryonic growth in vitro. Br Med Bull. 1990;46(3):675–94.

    CAS  PubMed  Google Scholar 

  110. Papi M, Brunelli R, Familiari G, Frassanito MC, Lamberti L, Maulucci G, et al. Whole-depth change in bovine zona pellucida biomechanics after fertilization: how relevant in hindering polyspermy? PLoS One. 2012;7(9):e45696.

    CAS  PubMed Central  PubMed  Google Scholar 

  111. Hunter RH. Sperm-egg interactions in the pig: monospermy, extensive polyspermy, and the formation of chromatin aggregates. J Anat. 1976;122(Pt 1):43–59.

    CAS  PubMed Central  PubMed  Google Scholar 

  112. Hunter RH. Oviduct function in pigs, with particular reference to the pathological condition of polyspermy. Mol Reprod Dev. 1991;29(4):385–91.

    CAS  PubMed  Google Scholar 

  113. Sato K. Polyspermy-preventing mechanisms in mouse eggs fertilized in vitro. J Exp Zool. 1979;210(2):353–9.

    CAS  PubMed  Google Scholar 

  114. Stewart-Savage J, Bavister BD. A cell surface block to polyspermy occurs in golden hamster eggs. Dev Biol. 1988;128(1):150–7.

    CAS  PubMed  Google Scholar 

  115. Ducibella T. The cortical reaction and development of activation competence in mammalian oocytes. Hum Reprod Update. 1996;2(1):29–42.

    CAS  PubMed  Google Scholar 

  116. Gahlay G, Gauthier L, Baibakov B, Epifano O, Dean J. Gamete recognition in mice depends on the cleavage status of an egg’s zona pellucida protein. Science. 2010;329(5988): 216–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  117. Burkart AD, Xiong B, Baibakov B, Jimenez-Movilla M, Dean J. Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy. J Cell Biol. 2012;197(1):37–44.

    CAS  PubMed Central  PubMed  Google Scholar 

  118. Wang WH, Day BN, Wu GM. How does polyspermy happen in mammalian oocytes? Microsc Res Tech. 2003;61(4):335–41.

    PubMed  Google Scholar 

  119. Melandri F, Grenier L, Plamondon L, Huskey WP, Stein RL. Kinetic studies on the inhibition of isopeptidase T by ubiquitin aldehyde. Biochemistry. 1996;35(39):12893–900.

    CAS  PubMed  Google Scholar 

  120. Hershko A, Rose IA. Ubiquitin-aldehyde: a general inhibitor of ubiquitin-recycling processes. Proc Natl Acad Sci U S A. 1987;84(7):1829–33.

    CAS  PubMed Central  PubMed  Google Scholar 

  121. Saigoh K, Wang YL, Suh JG, Yamanishi T, Sakai Y, Kiyosawa H, et al. Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat Genet. 1999;23(1): 47–51.

    CAS  PubMed  Google Scholar 

  122. Kondoh E, Konno A, Inaba K, Oishi T, Murata M, Yoshida M. Valosin-containing protein/p97 interacts with sperm-activating and sperm-attracting factor (SAAF) in the ascidian egg and modulates sperm-attracting activity. Dev Growth Differ. 2008;50(8):665–73.

    CAS  PubMed  Google Scholar 

  123. Kurihara LJ, Kikuchi T, Wada K, Tilghman SM. Loss of Uch-L1 and Uch-L3 leads to neurodegeneration, posterior paralysis and dysphagia. Hum Mol Genet. 2001;10(18):1963–70.

    CAS  PubMed  Google Scholar 

  124. Sutovsky P, Manandhar G, McCauley TC, Caamano JN, Sutovsky M, Thompson WE, et al. Proteasomal interference prevents zona pellucida penetration and fertilization in mammals. Biol Reprod. 2004;71(5):1625–37.

    CAS  PubMed  Google Scholar 

  125. Morales P, Kong M, Pizarro E, Pasten C. Participation of the sperm proteasome in human fertilization. Hum Reprod. 2003;18(5):1010–7.

    CAS  PubMed  Google Scholar 

  126. Doelling JH, Phillips AR, Soyler-Ogretim G, Wise J, Chandler J, Callis J, et al. The ubiquitin-specific protease subfamily UBP3/UBP4 is essential for pollen development and transmission in Arabidopsis. Plant Physiol. 2007;145(3):801–13.

    CAS  PubMed Central  PubMed  Google Scholar 

  127. Assou S, Cerecedo D, Tondeur S, Pantesco V, Hovatta O, Klein B, et al. A gene expression signature shared by human mature oocytes and embryonic stem cells. BMC Genomics. 2009;10:10.

    PubMed Central  PubMed  Google Scholar 

  128. Yamazaki K, Wakasugi N, Sakakibara A, Tomita T. Reduced fertility in gracile axonal dystrophy (gad) mice. Jikken Dobutsu. 1988;37(2):195–9.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by a grant from the National Institutes of Health, National Institute of Child Health and Human Development, HD 43092 to Keith E. Latham, by Agriculture and Food Research Initiative Competitive Grant no. 2011-67015-20025 from the USDA National Institute of Food and Agriculture to Peter Sutovsky, and by seed funding from the Food for the Twenty-first Century Program of the University of Missouri to Peter Sutovsky.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Namdori R. Mtango .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Mtango, N.R., Latham, K.E., Sutovsky, P. (2014). Deubiquitinating Enzymes in Oocyte Maturation, Fertilization and Preimplantation Embryo Development. In: Sutovsky, P. (eds) Posttranslational Protein Modifications in the Reproductive System. Advances in Experimental Medicine and Biology, vol 759. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-0817-2_5

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-0817-2_5

  • Published:

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4939-0816-5

  • Online ISBN: 978-1-4939-0817-2

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics