Treatment with the Proteasome Inhibitor MG132 during the End of Oocyte Maturation Improves Oocyte Competence for Development after Fertilization in Cattle

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  You, Jinyoung ^a   Lee, Eunsong ^a   Bonilla, Luciano ^b   Francis, Jasmine ^b   Koh, Jin ^b   Block, Jeremy ^b,c   Chen, Sixue ^b   Hansen, Peter J ^b  

^a Kangwon National University   (South Korea)

^b UNIVERSITY OF FLORIDA   (United States)

^c Ovatech LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A ACETYLTRANSFERASE; ADENOSINE DIPHOSPHATE ADENOSINE TRIPHOSPHATE TRANSLOCASE 2; ADENOSYLHOMOCYSTEINASE; ADENYLOSUCCINATE LYASE; ASPARTATE AMMONIA LIGASE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BOVINE SERUM ALBUMIN; CULLIN ASSOCIATED NEDD8 DISSOCIATED PROTEIN 1; CYCLIN DEPENDENT KINASE 5; ELONGATION FACTOR 1 GAMMA; GLUTATHIONE TRANSFERASE M3; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN 90B1; HYPOXIA UPREGULATED PROTEIN 1; LACTADHERIN; MGP57 53 GLYCOPROTEIN; P4HB PROTEIN; PDIA3 PROTEIN; PEPTIDES AND PROTEINS; PHOSPHOLIPASE A2 ACTIVATING PROTEIN; PROTEIN DISULFIDE ISOMERASE A3; SOLUTE CARRIER FAMILY 25 MEMBER 5; STRESS INDUCED PHOSPHOPROTEIN 1; THIMET OLIGOPEPTIDASE 1; TUBULIN ALPHA1C; UBIQUITIN ACTIVATING ENZYME E1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLASTOCYST; CATTLE; CELL ORGANELLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CUMULUS OOPHORUS; DRUG EFFECT; EMBRYO; EMBRYO TRANSFER; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; GLYCOLYSIS; MEIOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE CLEAVAGE; OOCYTE DEVELOPMENT; OOCYTE MATURATION; PREGNANCY RATE; PROTEIN EXPRESSION; PROTEIN FOLDING;

ANIMALS; BLASTOCYST; CATTLE; CELL DIFFERENTIATION; CELL NUCLEUS; EMBRYO TRANSFER; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION; LEUPEPTINS; MEIOSIS; OOCYTES; PREGNANCY; PROTEASOME INHIBITORS; TIME FACTORS; TRANSCRIPTION FACTORS;

BOS; BOVINAE;

EID: 84868686519     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048613     Document Type: Article

References (48)

1. Karabinova P, Kubelka M, Susor A, (2011) Proteasomal degradation of ubiquitinated proteins in oocyte meiosis and fertilization in mammals. Cell Tissue Res 346: 1-9.
2. Yang Q, Allard P, Huang M, Zhang W, Clarke HJ, (2010) Proteasomal activity is required to initiate and to sustain translational activation of messenger RNA encoding the stem-loop-binding protein during meiotic maturation in mice. Biol Reprod 2010 82: 123-31.
3. Reverte CG, Ahearn MD, Hake LE, (2001) CPEB degradation during Xenopus oocyte maturation requires a PEST domain and the 26S proteasome. Dev Biol 231: 447-458.
4. Nagyova E, Scsukova S, Nemcova L, Mlynarcikova A, Yi YJ, et al. (2012) Inhibition of proteasomal proteolysis affects expression of extracellular matrix components and steroidogenesis in porcine oocyte-cumulus complexes. Domest Anim Endocrinol 42: 50-62.
5. Lee DH, Goldberg AL, (1998) Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol 8: 397-403.
6. Ono T, Mizutani E, Li C, Yamagata K, Wakayama T, (2011) Offspring from intracytoplasmic sperm injection of aged mouse oocytes treated with caffeine or MG132. Genesis 49: 460-471.
7. You J, Kim J, Lee H, Hyun SH, Hansen PJ, et al. (2012) MG132 treatment during oocyte maturation improves embryonic development after somatic cell nuclear transfer and alters oocyte and embryo transcript abundance in pigs. Mol Reprod Dev 79: 41-50.
8. Parrish JJ, Susko-Parrish JL, Leibfried-Rutledge ML, Critser ES, Eyestone WH, et al. (1986) Bovine in vitro fertilization with frozen-thawed semen. Theriogenology 25: 591-600.
9. Fields SD, Hansen PJ, Ealy AD, (2011) Fibroblast growth factor requirements for in vitro development of bovine embryos. Theriogenology 75: 1466-1475.
10. Law ME, Corsino PE, Jahn SC, Davis BJ, Chen S, et al. (2012) Glucocorticoids and histone deacetylase inhibitors cooperate to block the invasiveness of basal-like breast cancer cells through novel mechanisms. Oncogene, in press.
11. Shilov IV, Seymour SL, Patel AA, Loboda A, Tang WH, et al. (2007) The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteomics 2007 6: 1638-1655.
12. Koh J, Chen S, Zhu N. Yu F, Soltis PS, et al. (2012) Comparative proteomics of the recently and recurrently formed natural allopolyploid Tragopogon mirus (Asteraceae) and its parents. New Phytologist. 196: 292-305.
13. Fisher RA, (1948) Questions and answers #14. Am Stat 2: 30-31.
14. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics21: 3674-3676.
15. Huang DW, Sherman BT, Lempicki RA, (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13.
16. Chen H, Sharp BM, (2004) Content-rich biological network constructed by mining PubMed abstracts. BMC Bioinformatics 5: 147.
17. Sakatani M, Alvarez NV, Takahashi M, Hansen PJ, (2012) Consequences of physiological heat shock beginning at the zygote stage on embryonic development and expression of stress response genes in cattle. J Dairy Sci 95: 3080-3091.
18. Block J, Bonilla L, Hansen PJ, (2010) Efficacy of in vitro embryo transfer in lactating dairy cows using fresh or vitrified embryos produced in a novel embryo culture medium. J Dairy Sci 93: 5234-5242.
19. Robertson I, Nelson RE. (1998) Certification and identification of the embryo. Pages 103-116 in Manual of the International Embryo Transfer Society. 3rd ed. DA Stringfellow and SE Seidel, ed. IETS, Champaign, IL.
20. Brusveen DJ, Cunha AP, Silva CD, Cunha PM, Sterry RA, et al. (2008) Altering the time of the second gonadotropin-releasing hormone injection and artificial insemination (AI) during Ovsynch affects pregnancies per AI in lactating dairy cows. J Dairy Sci 91: 1044-1052.
21. Demant M, Trapphoff T, Fröhlich T, Arnold GJ, Eichenlaub-Ritter U, (2012) Vitrification at the pre-antral stage transiently alters inner mitochondrial membrane potential but proteome of in vitro grown and matured mouse oocytes appears unaffected. Hum Reprod 27: 1096-1111.
22. Gao S, Han Z, Kihara M, Adashi E, Latham KE, (2005) Protease inhibitor MG132 in cloning: no end to the nightmare. Trends Biotechnol 23: 66-68.
23. Wu YG, Zhou P, Lan GC, Wang G, Luo MJ, et al. (2007) The effects of delayed activation and MG132 treatment on nuclear remodeling and preimplantation development of embryos cloned by electrofusion are correlated with the age of recipient cytoplasts. Cloning Stem Cells 9: 417-431.
24. Mizumoto S, Kato Y, Tsunoda Y, (2008) The developmental potential of parthenogenetic and somatic cell nuclear-transferred rat oocytes in vitro. Cloning Stem Cells 10: 4453-4459.
25. Nakajima N, Inomata T, Kashiwazaki N, (2008) Treatment with proteasome inhibitor MG132 during cloning improves survival and pronuclear number of reconstructed rat embryos. Cloning Stem Cells 10: 461-468.
26. Whitworth KM, Li R, Spate LD, Wax DM, Rieke A, et al. (2009) Method of oocyte activation affects cloning efficiency in pigs. Mol Reprod Dev 76: 490-500.
27. You J, Lee J, Kim J, Park J, Lee E, (2010) Post-fusion treatment with MG132 increases transcription factor expression in somatic cell nuclear transfer embryos in pigs. Mol Reprod Dev 77: 149-157.
28. Wagner SA, Beli P, Weinert BT, Nielsen ML, Cox J, et al. (2011) A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 10: M111.013284.
29. Berendt FJ, Fröhlich T, Bolbrinker P, Boelhauve M, Güngör T, et al. (2009) Highly sensitive saturation labeling reveals changes in abundance of cell cycle-associated proteins and redox enzyme variants during oocyte maturation in vitro. Proteomics 9: 550-564.
30. Mamo S, Carter F, Lonergan P, Leal CL, Al Naib A, et al. (2011) Sequential analysis of global gene expression profiles in immature and in vitro matured bovine oocytes: potential molecular markers of oocyte maturation. BMC Genomics 12: 151.
31. Blumenfeld N, Gonen H, Mayer A, Smith CE, Siegel NR, et al. (1994) Purification and characterization of a novel species of ubiquitin-carrier protein, E2, that is involved in degradation of non-"N-end rule" protein substrates. J Biol Chem 269: 9574-9581.
32. Yun JW, Kim SK, Kim H, (2011) Prolonged protein turnover of glyceraldehyde-3-phosphate dehydrogenase by phospholipase C-gamma 1 is critical for anchorage-independent growth and ATP synthesis in transformed cells. Cancer Invest 29: 93-101.
33. Duda DM, Scott DC, Calabrese MF, Zimmerman ES, Zheng N, et al. (2011) Structural regulation of cullin-RING ubiquitin ligase complexes. Curr Opin Struct Biol 21: 257-264.
34. Sutton-McDowall ML, Gilchrist RB, Thompson JG, (2010) The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139: 685-695.
35. Krisher RL, Bavister BD, (1999) Enhanced glycolysis after maturation of bovine oocytes in vitro is associated with increased developmental competence. Mol Reprod Dev 53: 19-26.
36. Albertini DF, (1992) Cytoplasmic microtubular dynamics and chromatin organization during mammalian oogenesis and oocyte maturation. Mutat Res 296: 57-68.
37. Rivera RM, Kelley KL, Erdos GW, Hansen PJ, (2004) Reorganization of microfilaments and microtubules by thermal stress in two-cell bovine embryos. Biol Reprod 70: 1852-1862.
38. Noiva R, (1999) Protein disulfide isomerase: the multifunctional redox chaperone of the endoplasmic reticulum. Semin Cell Dev Biol 10: 481-493.
39. Park J, Easton DP, Chen X, MacDonald IJ, Wang XY, et al. (2003) The chaperoning properties of mouse grp170, a member of the third family of hsp70 related proteins. Biochemistry 42: 14893-14902.
40. Roth Z, Hansen PJ, (2004) Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol Reprod 71: 1898-1906.
41. Cui H, Darmanin S, Natsuisaka M, Kondo T, Asaka M, et al. (2007) Enhanced expression of asparagine synthetase under glucose-deprived conditions protects pancreatic cancer cells from apoptosis induced by glucose deprivation and cisplatin. Cancer Res 67: 3345-3355.
42. Usmani SZ, Bona RD, Chiosis G, Li Z, (2010) The anti-myeloma activity of a novel purine scaffold HSP90 inhibitor PU-H71 is via inhibition of both HSP90A and HSP90B1. J Hematol Oncol 3: 40.
43. Pahl HL, (1999) Signal transduction from the endoplasmic reticulum to the cell nucleus Physiol Rev. 79: 683-701.
44. Shirogane T, Fukada T, Muller JM, Shima DT, Hibi M, et al. (1999) Synergistic roles for Pim-1 and c-Myc in STAT3-mediated cell cycle progression and antiapoptosis. Immunity 11: 709-719.
45. Lopes JP, Oliveira CR, Agostinho P, (2010) Neurodegeneration in an Aβ-induced model of Alzheimer's disease: the role of Cdk5. Aging Cell 9: 64-77.
46. Hashida T, Kotake Y, Ohta S, (2011) Protein disulfide isomerase knockdown-induced cell death is cell-line-dependent and involves apoptosis in MCF-7 cells. J Toxicol Sci 36: 1-7.
47. Kondoh E, Konno A, Inaba K, Oishi T, Murata M, et al. (2008) 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 50: 665-673.
48. Sutovsky P, (2011) Sperm proteasome and fertilization. Reproduction 142: 1-14.