Histone deacetylase inhibitor trichostatin A affects porcine oocyte maturation in vitro
Yong-Xun Jin A , Ming-Hui Zhao A , Zhong Zheng A B , Jung-Suk Kwon A , Seul-Ki Lee A , Xiang-Shun Cui A C and Nam-Hyung Kim A C
+ Author Affiliations
- Author Affiliations
A Department of Animal Sciences, Chungbuk National University, Cheong-Ju, 361-763, South Korea.
B College of Veterinary Medicine, Chungbuk National University, Cheong-Ju, 361-763, South Korea.
C Corresponding authors. Emails: nhkim@chungbuk.ac.kr; xscui@chungbuk.ac.kr
Reproduction, Fertility and Development 26(6) 806-816 https://doi.org/10.1071/RD13013
Submitted: 15 January 2013 Accepted: 13 May 2013 Published: 13 June 2013
Abstract
Previous studies show that porcine oocyte aging resulting from asynchronised IVM impairs embryo developmental competence. In the present study we investigated whether trichostatin A (TSA; an inhibitor of histone deacetylation) prolongs the maturation time and prevents the aging of oocytes. Porcine oocytes were cultured in medium containing increasing concentrations of TSA (300 nM) for 24, 44 or 64 h. The percentage of oocytes that underwent germinal vesicle breakdown was significantly lower in the TSA-treated group (300 nM) than in the control group. TSA did not affect oocyte quality at MII based on levels of maturation-promoting factor, the phosphorylation status of mitogen-activated protein kinase or histone H3K9 acetylation analysis. We also compared the preimplantation developmental competence and the viability of pathenogenetic embryos treated with 100 nM TSA for 24 h and then continuously cultured for another 24 h in TSA free condition. No significant differences were observed for either parameter between the TSA-treated and control groups. These results indicate that TSA prolongs the IVM of porcine oocytes but that oocyte quality and aging are not affected. These findings provide a feasible option by which to adjust the initiation time of downstream experiments based on porcine matured oocytes.
Additional keywords: acetylation, histone H3K9, oocyte aging, p-MAPK, prolong.
References
Akiyama, T., Nagata, M., and Aoki, F. (2006). Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. Proc. Natl Acad. Sci. USA 103, 7339–7344.| Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkslOrs70%3D&md5=7522191a2eb146e50f5040d1a7efcbfeCAS | 16651529PubMed |
Betts, D. H., and King, W. A. (2001). Genetic regulation of embryo death and senescence. Theriogenology 55, 171–191.
| Genetic regulation of embryo death and senescence.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7nslartw%3D%3D&md5=74db08e7d856d8abce04fb4cad25c7beCAS | 11198081PubMed |
Boise, L. H., Gonzales-Garcia, M., Postema, C. E., Ding, L. A., Lindsten, T., Turka, L., Mao, X., Nunerz, G., and Thompson, C. B. (1993). Bcl-x, a bcl-2 related gene that functions as a dominant regulator of apoptotic cell death. Cell 74, 597–608.
| Bcl-x, a bcl-2 related gene that functions as a dominant regulator of apoptotic cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmsVans7g%3D&md5=12038927b77f27a0c13af3912fabf88eCAS | 8358789PubMed |
Bornslaeger, E. A., Mattei, P., and Schultz, R. M. (1986). Involvement of cAMP-dependent protein kinase and protein phosphorylation in regulation of mouse oocyte maturation. Dev. Biol. 114, 453–462.
| Involvement of cAMP-dependent protein kinase and protein phosphorylation in regulation of mouse oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xhs1KisLk%3D&md5=beeb027da1680bfa71cf8ce76396f141CAS | 2420661PubMed |
De La Fuente, R., Viveiros, M. M., Burns, K. H., Adashi, E. Y., Matzuk, M. M., and Eppig, J. J. (2004). Major chromatin remodeling in the germinal vesicle of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. Dev. Biol. 275, 447–458.
| Major chromatin remodeling in the germinal vesicle of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVKltbc%3D&md5=b3a4dc4df912c16d3a904a7c20b55726CAS | 15501230PubMed |
Endo, T., Naito, K., Aoki, F., Kume, S., and Tojo, H. (2005). Changes in histone modifications during in vitro maturation of porcine oocytes. Mol. Reprod. Dev. 71, 123–128.
| Changes in histone modifications during in vitro maturation of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtVOqs7w%3D&md5=8782e3cb35e916c793edb6bf5e03225aCAS | 15736133PubMed |
Endo, T., Kano, K., and Naito, K. (2008). Nuclear histone deacetylases are not required for global histone deacetylation during meiotic maturation in porcine oocytes. Biol. Reprod. 78, 1073–1080.
| Nuclear histone deacetylases are not required for global histone deacetylation during meiotic maturation in porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVWktbw%3D&md5=21752469b24b3dbb70dfa22ce394b135CAS | 18305223PubMed |
Fan, H. Y., and Sun, Q. Y. (2004). Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol. Reprod. 70, 535–547.
| Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Chsro%3D&md5=3346fa70e84ef833806d623093c90069CAS | 14613897PubMed |
Fujino, Y., Ozaki, K., Yamamasu, S., Ito, F., Matsuoka, I., Hayashi, E., Nakamura, H., Ogita, S., Sato, E., and Inoue, M. (1996). DNA fragmentation of oocytes in aged mice. Hum. Reprod. 11, 1480–1483.
| DNA fragmentation of oocytes in aged mice.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28zisVKqsg%3D%3D&md5=fa9856b5f4559fc4780097cca8722db3CAS | 8671488PubMed |
Funahashi, H., Cantley, T. C., and Day, B. N. (1997). Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization. Biol. Reprod. 57, 49–53.
| Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktFCntb0%3D&md5=47d8032577a493be5bdbfd87fda7a9a2CAS | 9209079PubMed |
Gordo, A. C., Rodrigues, P., Kurokawa, M., Jellerette, T., Exley, G. E., Warner, C., and Fissore, R. (2002). Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs. Biol. Reprod. 66, 1828–1837.
| Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvFensrw%3D&md5=a7e44fdd7005c366a30da81de41fe29bCAS | 12021069PubMed |
Göttlicher, M., Minucci, S., Zhu, P., Kramer, O. H., Schimpf, A., Giavara, S., Sleeman, J. P., Lo Coco, F., Nervi, C., Pelicci, P. G., and Heinzel, T. (2001). Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J. 20, 6969–6978.
| Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells.Crossref | GoogleScholarGoogle Scholar | 11742974PubMed |
Hao, Y., Lai, L., Mao, J., Im, G. S., Bonk, A., and Prather, R. S. (2004). Apoptosis in parthenogenetic preimplantation porcine embryos. Biol. Reprod. 70, 1644–1649.
| Apoptosis in parthenogenetic preimplantation porcine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOmtrw%3D&md5=58a011096351b08a67a48cd888ef4987CAS | 14766725PubMed |
Ivanovska, I., and Orr-Weaver, T. L. (2006). Histone modifications and the chromatin scaffold for meiotic chromosome architecture. Cell Cycle 5, 2064–2071.
| Histone modifications and the chromatin scaffold for meiotic chromosome architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlGqsr%2FE&md5=1ac9411d62b300cd11be726210cd5f8bCAS | 16969105PubMed |
Ješeta, M., Petr, J., Krejcova, T., Chmelikova, E., and Jilek, F. (2008). In vitro ageing of pig oocytes: effects of the histone deacetylase inhibitor trichostatin A. Zygote 16, 145–152.
| In vitro ageing of pig oocytes: effects of the histone deacetylase inhibitor trichostatin A.Crossref | GoogleScholarGoogle Scholar | 18405435PubMed |
Jin, Y. X., Cui, X. S., Han, Y. J., and Kim, N. H. (2009). Leptin accelerates pronuclear formation following intracytoplasmic sperm injection of porcine oocytes: possible role for MAP kinase inactivation. Anim. Reprod. Sci. 115, 137–148.
| Leptin accelerates pronuclear formation following intracytoplasmic sperm injection of porcine oocytes: possible role for MAP kinase inactivation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptl2iuro%3D&md5=59f5d02c1181ae3467a3ea8d53753bd8CAS | 19100691PubMed |
Kikuchi, K., Izaike, Y., Noguchi, J., Furukawa, T., Daen, F. P., Naito, K., and Toyoda, Y. (1995). Decrease of histone H1 kinase activity in relation to parthenogenetic activation of pig follicular oocytes matured and aged in vitro. J. Reprod. Fertil. 105, 325–330.
| Decrease of histone H1 kinase activity in relation to parthenogenetic activation of pig follicular oocytes matured and aged in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjslSntw%3D%3D&md5=98c224e7f134529c3185ca054a520792CAS | 8568778PubMed |
Kikuchi, K., Naito, K., Noguchi, J., Shimada, A., Kaneko, H., Yamashita, M., Aoki, F., Tojo, H., and Toyoda, Y. (2000). Maturation/M-phase promoting factor: a regulator of aging in porcine oocytes. Biol. Reprod. 63, 715–722.
| Maturation/M-phase promoting factor: a regulator of aging in porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtFCitbc%3D&md5=8689f17eb4a755d6e82501bb84bc085aCAS | 10952912PubMed |
Kim, J. S., Cho, Y. S., Song, B. S., Wee, G., Park, J. S., Choo, Y. K., Yu, K., Lee, K. K., Han, Y. M., and Koo, D. B. (2008). Exogenous dibutyryl cAMP affects meiotic maturation via protein kinase A activation; it stimulates further embryonic development including blastocyst quality in pigs. Theriogenology 69, 290–301.
| Exogenous dibutyryl cAMP affects meiotic maturation via protein kinase A activation; it stimulates further embryonic development including blastocyst quality in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvV2itQ%3D%3D&md5=ac3340df02ac249e831a5a9155a95d14CAS | 17977589PubMed |
Kim, N. H., Moon, S. J., Prather, R. S., and Day, B. N. (1996). Cytoskeletal alteration in aged porcine oocytes and parthenogenesis. Mol. Reprod. Dev. 43, 513–518.
| Cytoskeletal alteration in aged porcine oocytes and parthenogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitVGjsLw%3D&md5=1dc64886c754225828bdeedb97c847d5CAS | 9052943PubMed |
Krämer, O. H., Zhu, P., Ostendorff, H. P., Golebiewski, M., Tiefenbach, J., Peters, M. A., Brill, B., Groner, B., Bach, I., Heinzel, T., and Göttlicher, M. (2003). The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2. EMBO J. 22, 3411–3420.
| The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2.Crossref | GoogleScholarGoogle Scholar | 12840003PubMed |
Kuroda, T., Naito, K., Sugiura, K., Yamashita, M., Takakura, I., and Tojo, H. (2004). Analysis of the roles of cyclin B1 and cyclin B2 in porcine oocyte maturation by inhibiting synthesis with antisense RNA injection. Biol. Reprod. 70, 154–159.
| Analysis of the roles of cyclin B1 and cyclin B2 in porcine oocyte maturation by inhibiting synthesis with antisense RNA injection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvV2m&md5=74f74ed7a69e9fbb680d01a3feea3ea8CAS | 12954723PubMed |
Levy, R. R., Cordonier, H., Czyba, J. C., and Guerin, J. F. (2001). Apoptosis in preimplantation mammalian embryo and genetics. Ital. J. Anat. Embryol. 106, 101–108..
| 1:STN:280:DC%2BD3MnosF2rtw%3D%3D&md5=673bc2e96db1425943881cb11bf4ca97CAS | 11732565PubMed |
Liu, L., and Keefe, D. L. (2002). Ageing-associated aberration in meiosis of oocytes from senescence-accelerated mice. Hum. Reprod. 17, 2678–2685.
| Ageing-associated aberration in meiosis of oocytes from senescence-accelerated mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xns1GgtL0%3D&md5=02d0e0769c4c8f172d7ba4233cb8740cCAS | 12351548PubMed |
Mailhes, J. B., Young, D., and London, S. N. (1998). Postovulatory ageing of mouse oocytes in vitro and premature centromere separation and aneuploidy. Biol. Reprod. 58, 1206–1210.
| Postovulatory ageing of mouse oocytes in vitro and premature centromere separation and aneuploidy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivFClsLo%3D&md5=2f3a19913057e776618f7deabf294ef9CAS | 9603254PubMed |
Meinecke, B., and Krischek, C. (2003). MAPK/ERK kinase (MEK) signalling is required for resumption of meiosis in cultured cumulus-enclosed pig oocytes. Zygote 11, 7–16.
| MAPK/ERK kinase (MEK) signalling is required for resumption of meiosis in cultured cumulus-enclosed pig oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1Wgsrk%3D&md5=edc8e4d6a79e0df7c6b3f699987a86cdCAS | 12625524PubMed |
Perez, G. I., Tao, X. J., and Tilly, J. L. (1999). Fragmentation and death (a.k.a. apoptosis) of ovulated oocytes. Mol. Hum. Reprod. 5, 414–420.
| Fragmentation and death (a.k.a. apoptosis) of ovulated oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3mvVKrtA%3D%3D&md5=b6ffb5937c831632a950f9c6fdd64d54CAS | 10338364PubMed |
Richard, F. J. (2007). Regulation of meiotic maturation. J. Anim. Sci. 85, E4–E6.
| Regulation of meiotic maturation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s7itlWgsQ%3D%3D&md5=7b80ed45753edc22b6ecfccc63d2e5a1CAS | 17040950PubMed |
Schramm, R. D., Paprocki, A. M., and Bavister, B. D. (2002). Features associated with reproductive ageing in female rhesus monkeys. Hum. Reprod. 17, 1597–1603.
| Features associated with reproductive ageing in female rhesus monkeys.Crossref | GoogleScholarGoogle Scholar | 12042284PubMed |
Shojo, A., Tatemoto, H., and Terada, T. (2000). Effect of aging on parthenogenetic activation with cycloheximide and alteration of the activity of maturation promoting factor during aging of bovine oocytes. J. Mamm. Ova Res. 17, 35–41.
Sugiura, K., Naito, K., Endo, T., and Tojo, H. (2006). Study of germinal vesicle requirement for the normal kinetics of maturation/M-phase-promoting factor activity during porcine oocyte maturation. Biol. Reprod. 74, 593–600.
| Study of germinal vesicle requirement for the normal kinetics of maturation/M-phase-promoting factor activity during porcine oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhslejsLk%3D&md5=2d52221ce5e43f7d0c7d14cba899adeeCAS | 16319287PubMed |
Sun, S. C., Gao, W. W., Xu, Y. N., Jin, Y. X., Wang, Q. L., Yin, X. J., Cui, X. S., and Kim, N. H. (2012). Degradation of actin nucleators affects cortical polarity of aged mouse oocytes. Fertil. Steril. 97, 984–990.
| Degradation of actin nucleators affects cortical polarity of aged mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvF2jtL4%3D&md5=e2043e2731ab7ce980767b7daec49824CAS | 22306711PubMed |
Voronina, E., and Wessel, G. M. (2003). The regulation of oocyte maturation. Curr. Top. Dev. Biol. 58, 53–110.
| The regulation of oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFaqtbs%3D&md5=e2eae933848c582b29fafc677d27389dCAS | 14711013PubMed |
Wang, Q., Wang, C. M., Ai, J. S., Xiong, B., Yin, S., Hou, Y., Chen, D. Y., Schatten, H., and Sun, Q. Y. (2006a). Histone phosphorylation and pericentromeric histone modifications in oocyte meiosis. Cell Cycle 5, 1974–1982.
| Histone phosphorylation and pericentromeric histone modifications in oocyte meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWqsLjI&md5=fac71c15c8f75a198efec3f28f66170fCAS | 16969090PubMed |
Wang, Q., Yin, S., Ai, J. S., Liang, C. G., Hou, Y., Chen, D. Y., Schatten, H., and Sun, Q. Y. (2006b). Histone deacetylation is required for orderly meiosis. Cell Cycle 5, 766–774.
| Histone deacetylation is required for orderly meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvVCju74%3D&md5=d8438e0b988df4682e5f0d7f3c48ec70CAS | 16582639PubMed |
Wetzel, M., Premkumar, D. R. D., Arnold, B., and Pollack, I. F. (2005). Effect of trichostatin A, a histone deacetylase inhibitor, on glioma proliferation in vitro by inducing cell cycle arrest and apoptosis. J. Neurosurg. 103, 549–556..
| 16383255PubMed |
Wilcox, A. J., Weinberg, C. R., and Baird, D. D. (1998). Post-ovulatory ageing of the human oocyte and embryo failure. Hum. Reprod. 13, 394–397.
| Post-ovulatory ageing of the human oocyte and embryo failure.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3hs12htg%3D%3D&md5=6033cd85f22e1909622ef8ccde74c491CAS | 9557845PubMed |
