Protein deubiquitination during oocyte maturation influences sperm function during fertilisation, antipolyspermy defense and embryo development

Reproduction, Fertility and Development

Volumn 27, Issue 8, 2015, Pages 1154-1167

  Yi, Young Joo ^a,c   Sutovsky, Miriam ^a   Song, Won Hee ^a   Sutovsky, Peter ^a,b  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

^c Chonbuk National University   (South Korea)

Author keywords

pig; ubiquitin; UCHL1; UCHL3

Indexed keywords

1,3 INDANDIONE DERIVATIVE; ESTERASE INHIBITOR; ISATIN O ACYL OXIME; LUNG RESISTANCE PROTEIN; OXIME DERIVATIVE; UBIQUITIN C TERMINAL HYDROLASE L1; UBIQUITIN C TERMINAL HYDROLASE L3; UBIQUITIN THIOLESTERASE; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG; CYSTEINE PROTEINASE INHIBITOR;

AGGRESOME; ANTIPOLYSPERMY DEFENSE; ARTICLE; AUTOPHAGOSOME; BLASTOCYST; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO TRANSFER; ENZYME INHIBITION; FEMALE; FEMALE GENITAL SYSTEM FUNCTION; FERTILIZATION; GERMINAL VESICLE; HUMAN; HUMAN CELL; MEIOTIC SPINDLE; MITOCHONDRION; MITOPHAGY; NONHUMAN; OOCYTE CORTEX; OOCYTE MATURATION; POLYSPERMY; PREIMPLANTATION EMBRYO; PROTEIN ANALYSIS; PROTEIN DEUBIQUITINATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEOMICS; SPERMATOZOON PENETRATION; UBIQUITINATION; ZONA PELLUCIDA; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; MALE; OOCYTE; PHYSIOLOGY; PIG; PREGNANCY; SPERMATOZOON;

ANIMALS; CYSTEINE PROTEINASE INHIBITORS; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION; MALE; OOCYTES; PREGNANCY; PROTEOMICS; SPERMATOZOA; SWINE; UBIQUITIN THIOLESTERASE;

EID: 84943809189     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD14012     Document Type: Article

References (59)

1. Abeydeera, L. R., Wang, W. H., Prather, R. S., and Day, B. N. (1998). Maturation in vitro of pig oocytes in protein-free culture media: fertilization and subsequent embryo development in vitro. Biol. Reprod. 58, 1316-1320. doi:10.1095/BIOLREPROD58.5.1316
2. Al Rawi, S., Louvet-Vallee, S., Djeddi, A., Sachse, M., Culetto, E., Hajjar, C., Boyd, L., Legouis, R., and Galy, V. (2011). Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334, 1144-1147. doi:10.1126/SCIENCE. 1211878
3. Al Rawi, S., Louvet-Vallee, S., Djeddi, A., Sachse, M., Culetto, E., Hajjar, C., Boyd, L., Legouis, R., and Galy, V. (2012). Allophagy: a macro-autophagic process degrading spermatozoid-inherited organelles. Autophagy 8, 421-423. doi:10.4161/AUTO.19242
4. Altun, M., Kramer, H. B., Willems, L. I., McDermott, J. L., Leach, C. A., Goldenberg, S. J., Kumar, K. G., Konietzny, R., Fischer, R., Kogan, E., Mackeen, M. M., McGouran, J., Khoronenkova, S. V., Parsons, J. L., Dianov, G. L., Nicholson, B., and Kessler, B. M. (2011). Activity-based chemical proteomics accelerates inhibitor development for deubi-quitylating enzymes. Chem. Biol. 18, 1401-1412. doi:10.1016/J.CHEMBIOL.2011.08.018
5. Bheda, A., Gullapalli, A., Caplow, M., Pagano, J. S., and Shackelford, J. (2010). Ubiquitin editing enzyme UCH L1 and microtubule dynamics: implication in mitosis. Cell Cycle 9, 980-994. doi:10.4161/CC.9.5.10934
6. Bjørkøy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Øvervatn, A., Stenmark, H., and Johansen, T. (2005). p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171, 603-614. doi:10.1083/JCB.200507002
7. Chung, C. H., and Baek, S. H. (1999). Deubiquitinating enzymes: their diversity and emerging roles. Biochem. Biophys. Res. Commun. 266, 633-640. doi:10.1006/BBRC.1999.1880
8. D'Andrea, A., and Pellman, D. (1998). Deubiquitinating enzymes: a new class of biological regulators. Crit. Rev. Biochem. Mol. Biol. 33, 337-352. doi:10.1080/10409239891204251
9. Day, I. N., and Thompson, R. J. (1987). Molecular cloning of cDNA coding for human PGP 9.5 protein. A novel cytoplasmic marker for neurones and neuroendocrine cells. FEBS Lett. 210, 157-160. doi:10.1016/0014-5793(87)81327-3
10. Ellederova, Z., Halada, P., Man, P., Kubelka, M., Motlik, J., and Kovarova, H. (2004). Protein patterns of pig oocytes during in vitro maturation. Biol. Reprod. 71, 1533-1539. doi:10.1095/BIOLREPROD. 104.030304
11. Gong, L., Kamitani, T., Millas, S., and Yeh, E. T. (2000). Identification of a novel isopeptidase with dual specificity for ubiquitin-and NEDD8-conjugated proteins. J. Biol. Chem. 275, 14212-14 216. doi:10.1074/JBC.275.19.14212
12. Hjerpe, R., Aillet, F., Lopitz-Otsoa, F., Lang, V., England, P., and Rodriguez, M. S. (2009). Efficient protection and isolation of ubiquity-lated proteins using tandem ubiquitin-binding entities. EMBO Rep. 10, 1250-1258. doi:10.1038/EMBOR.2009.192
13. Huo, L.J., Fan, H. Y., Zhong, Z. S., Chen, D. Y., Schatten, H., and Sun, Q. Y. (2004). Ubiquitin-proteasome pathway modulates mouse oocyte meiotic maturation and fertilization via regulation of MAPK cascade and cyclin B1 degradation. Mech. Dev. 121, 1275-1287. doi:10.1016/J.MOD.2004.05.007
14. Huo, L. J., Zhong, Z. S., Liang, C. G., Wang, Q., Yin, S., Ai, J. S., Yu, L. Z., Chen, D. Y., Schatten, H., and Sun, Q. Y. (2006). 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. 11, 2193-2202. doi:10.2741/1961
15. Johansen, T., and Lamark, T. (2011). Selective autophagy mediated by autophagic adapter proteins. Autophagy 7, 279-296. doi:10.4161/AUTO.7.3.14487
16. Johnston, J. A., Ward, C. L., and Kopito, R. R. (1998). Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 143, 1883-1898. doi:10.1083/JCB.143.7.1883
17. Josefsberg, L. B., Galiani, D., Dantes, A., Amsterdam, A., and Dekel, N. (2000). The proteasome is involved in the first metaphase-to-anaphase transition of meiosis in rat oocytes. Biol. Reprod. 62, 1270-1277. doi:10.1095/BIOLREPROD62.5.1270
18. Kickhoefer, V. A., and Rome, L. H. (1994). The sequence of a cDNA encoding the major vault protein from Rattus norvegicus. Gene 151, 257-260. doi:10.1016/0378-1119(94)90667-X
19. Kolli, S., Zito, C. I., Mossink, M. H., Wiemer, E. A., and Bennett, A. M. (2004). The major vault protein is a novel substrate for the tyrosine phosphatase SHP-2 and scaffold protein in epidermal growth factor signaling. J. Biol. Chem. 279, 29 374-29 385. doi:10.1074/JBC.M313955200
20. Koyanagi, S., Hamasaki, H., Sekiguchi, S., Hara, K., Ishii, Y., Kyuwa, S., and Yoshikawa, Y. (2012). Effects of ubiquitin C-terminal hydrolase L1 deficiency on mouse ova. Reproduction 143, 271-279. doi:10.1530/REP-11-0128
21. Kurihara, L. J., Semenova, E., Levorse, J. M., and Tilghman, S. M. (2000). Expression and functional analysis of Uch-L3 during mouse development. Mol. Cell. Biol. 20, 2498-2504. doi:10.1128/MCB.20.7. 2498-2504.2000
22. Kurz, T., Pintard, L., Willis, J. H., Hamill, D. R., Gonczy, P., Peter, M., and Bowerman, B. (2002). Cytoskeletal regulation by the Nedd8 ubiquitin-like protein modification pathway. Science 295, 1294-1298. doi:10.1126/SCIENCE.1067765
23. Kwon, J., Kikuchi, T., Setsuie, R., Ishii, Y., Kyuwa, S., and Yoshikawa, Y. (2003). Characterization of the testis in congenitally ubiquitin carboxy-terminal hydrolase-1 (Uch-L1) defective (gad) mice.Exp. Anim.52, 1-9. doi:10.1538/EXPANIM.52.1
24. Kwon, J., Wang, Y. L., Setsuie, R., Sekiguchi, S., Sakurai, M., Sato, Y., Lee, W. W., Ishii, Y., Kyuwa, S., Noda, M., Wada, K., and Yoshikawa, Y. (2004). Developmental regulation of ubiquitin C-terminal hydrolase isozyme expression during spermatogenesis in mice. Biol. Reprod. 71, 515-521. doi:10.1095/BIOLREPROD. 104.027565
25. Li, L., Baibakov, B., and Dean, J. (2008). A subcortical maternal complex essential for preimplantation mouse embryogenesis. Dev. Cell 15, 416-425. doi:10.1016/J.DEVCEL.2008.07.010
26. Liu, Y., Lashuel, H. A., Choi, S., Xing, X., Case, A., Ni, J., Yeh, L. A., Cuny, G. D., Stein, R. L., and Lansbury, P. T., Jr. (2003). Discovery of inhibitors that elucidate the role of UCH-L1 activity in the H1299 lung cancer cell line. Chem. Biol. 10, 837-846. doi:10.1016/J.CHEMBIOL.2003.08.010
27. Mtango, N. R., and Latham, K. E. (2007). Ubiquitin proteasome pathway gene expression varies in rhesus monkey oocytes and embryos of different developmental potential. Physiol. Genomics 31, 1-14. doi:10.1152/PHYSIOLGENOMICS.00040.2007
28. Mtango, N. R., Sutovsky, M., Susor, A., Zhong, Z., Latham, K. E., and Sutovsky, P. (2012a). Essential role of maternal UCHL1 and UCHL3 in fertilization and preimplantation embryo development. J. Cell. Physiol. 227, 1592-1603. doi:10.1002/JCP.22876
29. Mtango, N. R., Sutovsky, M., Vandevoort, C. A., Latham, K. E., and Sutovsky, P. (2012b). Essential role of ubiquitin C-terminal hydrolases UCHL1 and UCHL3 in mammalian oocyte maturation. J. Cell. Physiol. 227, 2022-2029. doi:10.1002/JCP.22931
30. Novak, S., Paradis, F., Savard, C., Tremblay, K., and Sirard, M. A. (2004). Identification of porcine oocyte proteins that are associated with somatic cell nuclei after co-incubation. Biol. Reprod. 71, 1279-1289. doi:10.1095/BIOLREPROD.103.027037
31. Ohsugi, M., Zheng, P., Baibakov, B., Li, L., and Dean, J. (2008). Maternally derived FILIA-MATER complex localizes asymmetrically in cleavage-stage mouse embryos. Development 135, 259-269. doi:10.1242/DEV.011445
32. Pankiv, S., Clausen, T. H., Lamark, T., Brech, A., Bruun, J. A., Outzen, H., Overvatn, A., Bjorkoy, G., and Johansen, T. (2007). p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24 131-24 145. doi:10.1074/JBC.M702824200
33. Sato, M., and Sato, K. (2011). Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 334, 1141-1144. doi:10.1126/SCIENCE.1210333
34. Scheffer, G. L., Schroeijers, A. B., Izquierdo, M. A., Wiemer, E. A., and Scheper, R. J. (2000). Lung resistance-related protein/major vault protein and vaults in multidrug-resistant cancer. Curr. Opin. Oncol. 12, 550-556. doi:10.1097/00001622-200011000-00007
35. Seiberlich, V., Goldbaum, O., Zhukareva, V., and Richter-Landsberg, C. (2012). The small molecule inhibitor PR-619 of deubiquitinating enzymes affects the microtubule network and causes protein aggregate formation in neural cells: implications for neurodegenerative diseases. Biochim. Biophys. Acta 1823, 2057-2068. doi:10.1016/J.BBAMCR. 2012.04.011
36. Sekiguchi, S., Kwon, J., Yoshida, E., Hamasaki, H., Ichinose, S., Hideshima, M., Kuraoka, M., Takahashi, A., Ishii, Y., Kyuwa, S., Wada, K., and Yoshikawa, Y. (2006). Localization of ubiquitin C-terminal hydrolase L1 in mouse ova and its function in the plasma membrane to block polyspermy. Am. J. Pathol. 169, 1722-1729. doi:10.2353/AJPATH. 2006.060301
37. Sims, J. J., Scavone, F., Cooper, E. M., Kane, L. A., Youle, R. J., Boeke, J. D., and Cohen, R. E. (2012). Polyubiquitin-sensor proteins reveal localization and linkage-type dependence of cellular ubiquitin signaling. Nat. Methods 9, 303-309. doi:10.1038/NMETH.1888
38. Sun, Z. G., Kong, W. H., Zhang, Y. J., Yan, S., Lu, J. N., Gu, Z., Lin, F., and Tso, J. K. (2002). A novel ubiquitin carboxyl terminal hydrolase is involved in toad oocyte maturation. Cell Res. 12, 199-206. doi:10.1038/SJ.CR.7290125
39. Susor, A., Ellederova, Z., Jelinkova, L., Halada, P., Kavan, D., Kubelka, M., and Kovarova, H. (2007). Proteomic analysis of porcine oocytes during in vitro maturation reveals essential role for the ubiquitin C-terminal hydrolase-L1. Reproduction 134, 559-568. doi:10.1530/REP-07-0079
40. Susor, A., Liskova, L., Toralova, T., Pavlok, A., Pivonkova, K., Karabinova, P., Lopatarova, M., Sutovsky, P., and Kubelka, M. (2010). Role of ubiquitin C-terminal hydrolase-L1 in antipolyspermy defense of mammalian oocytes. Biol. Reprod. 82, 1151-1161. doi:10.1095/BIOLREPROD.109.081547
41. Sutovsky, P., Moreno, R. D., Ramalho-Santos, J., Dominko, T., Simerly, C., and Schatten, G. (1999). Ubiquitin tag for sperm mitochondria. Nature 402, 371-372. doi:10.1038/46466
42. Sutovsky, P., Moreno, R. D., Ramalho-Santos, J., Dominko, T., Simerly, C., and Schatten, G. (2000). Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol. Reprod. 63, 582-590. doi:10.1095/BIOLREPROD63.2.582
43. Sutovsky, P., McCauley, T. C., Sutovsky, M., and Day, B. N. (2003). Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biol. Reprod. 68, 1793-1800. doi:10.1095/BIOLREPROD.102.012799
44. Sutovsky, P., Manandhar, G., Laurincik, J., Letko, J., Caamaño, J. N., Day, B. N., Lai, L., Prather, R. S., Sharpe-Timms, L. L., Zimmer, R., and Sutovsky, M. (2005). Expression and proteasomal degradation of the major vault protein (MVP) in mammalian oocytes and zygotes. Reproduction 129, 269-282. doi:10.1530/REP.1.00291
45. Takebayashi, Y., Nakayama, K., Fujioka, T., Kanzaki, A., Mutho, M., Uchida, T., Miyazaki, K., Ito, M., and Fukumoto, M. (2001). Expression of multidrug resistance associated transporters (MDR1, MRP1, LRP and BCRP) in porcine oocyte. Int. J. Mol. Med. 7, 397-400.
46. Tian, X., Isamiddinova, N. S., Peroutka, R. J., Goldenberg, S. J., Mattern, M. R., Nicholson, B., and Leach, C. (2011). Characterization of selective ubiquitin and ubiquitin-like protease inhibitors using a fluorescence-based multiplex assay format. Assay Drug Dev. Technol. 9, 165-173. doi:10.1089/ADT.2010.0317
47. Tong, Z. B., Gold, L., Pfeifer, K. E., Dorward, H., Lee, E., Bondy, C. A., Dean, J., and Nelson, L. M. (2000). Mater, a maternal effect gene required for early embryonic development in mice. Nat. Genet. 26, 267-268. doi:10.1038/81547
48. van Wijk, S. J., Fiskin, E., Putyrski, M., Pampaloni, F., Hou, J., Wild, P., Kensche, T., Grecco, H. E., Bastiaens, P., and Dikic, I. (2012). Fluorescence-based sensors to monitor localization and functions of linear and K63-linked ubiquitin chains in cells. Mol. Cell 47, 797-809. doi:10.1016/J.MOLCEL.2012.06.017
49. Wada, H., Kito, K., Caskey, L. S., Yeh, E. T., and Kamitani, T. (1998). Cleavage of the C-terminus of NEDD8 by UCH-L3. Biochem. Biophys. Res. Commun. 251, 688-692. doi:10.1006/BBRC.1998.9532
50. Wilkinson, K. D. (1997). Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J. 11, 1245-1256.
51. Wilkinson, K. D. (2000). Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. Semin. Cell Dev. Biol. 11, 141-148. doi:10.1006/SCDB.2000.0164
52. Wilkinson, K. D., Lee, K. M., Deshpande, S., Duerksen-Hughes, P., Boss, J. M., and Pohl, J. (1989). The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246, 670-673. doi:10.1126/SCIENCE.2530630
53. Wilkinson, K. D., Deshpande, S., and Larsen, C. N. (1992). Comparisons of neuronal (PGP 9.5) and non-neuronal ubiquitin C-terminal hydrolases. Biochem. Soc. Trans. 20, 631-637.
54. Wójcik, C. (2002). Regulation of apoptosis by the ubiquitin and proteasome pathway. J. Cell. Mol. Med. 6, 25-48. doi:10.1111/J.1582-4934.2002. TB00309.X
55. Wójcik, C., Schroeter, D., Wilk, S., Lamprecht, J., and Paweletz, N. (1996). Ubiquitin-mediated proteolysis centers in HeLa cells: indication from studies of an inhibitor of the chymotrypsin-like activity of the protea-some. Eur. J. Cell Biol. 71, 311-318.
56. Yi, Y. J., Manandhar, G., Sutovsky, M., Li, R., Jonakova, V., Oko, R., Park, C. S., Prather, R. S., and Sutovsky, P. (2007). Ubiquitin C-terminal hydrolase-activity is involved in sperm acrosomal function and anti-polyspermy defense during porcine fertilization. Biol. Reprod. 77, 780-793. doi:10.1095/BIOLREPROD.107.061275
57. Yi, Y. J., Nagyova, E., Manandhar, G., Prochazka, R., Sutovsky, M., Park, C. S., and Sutovsky, P. (2008). 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. 78, 115-126. doi:10.1095/BIOLREPROD.107.061366
58. Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I. M., and Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112-119. doi:10.1095/BIOLREPROD66.1.112
59. Zhang, N., Wilkinson, K., and Bownes, M. (1993). Cloning and analysis of expression of a ubiquitin carboxyl terminal hydrolase expressed during oogenesis in Drosophila melanogaster. Dev. Biol. 157, 214-223. doi:10.1006/DBIO.1993.1125