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The potential roles of c-Jun N-terminal kinase (JNK) during the maturation and aging of oocytes produced by a marine protostome worm

Published online by Cambridge University Press:  16 October 2017

Stephen A. Stricker  and
Niharika Ravichandran
Stephen A. Stricker*
Affiliation:
Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA.
Niharika Ravichandran
Affiliation:
Department of Biology, University of New Mexico, Albuquerque, NM 87131USA.
*
All correspondence to: Stephen A. Stricker. Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA. Tel: +1 505 2771883. Fax: +1 505 2770304. E-mail: sstr@um.edu
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Summary

Previous investigations have indicated that c-Jun N-terminal kinase (JNK) regulates the maturation and aging of oocytes produced by deuterostome animals. In order to assess the roles of this kinase in a protostome, oocytes of the marine nemertean worm Cerebratulus were stimulated to mature and subsequently aged before being probed with phospho-specific antibodies against active forms of JNK and maturation-promoting factor (MPF). Based on blots of maturing oocytes, a 40-kD putative JNK is normally activated during germinal vesicle breakdown (GVBD), which begins at 30 min post-stimulation with seawater, whereas treating immature oocytes with JNK inhibitors downregulates both the 40-kD JNK signal and GVBD, collectively suggesting a 40-kD JNK may facilitate oocyte maturation. Along with this JNK activity, mature oocytes also exhibit high levels of MPF at 2 h post-stimulation. However, by ~6–8 h post-GVBD, mature oocytes lose the 40-kD JNK signal, and at ~20–30 h of aging, an ~48-kD phospho-JNK band arises as oocytes deactivate MPF and begin to lyse during a necroptotic-like mode of death. Accordingly, JNK inhibitors reduce the aging-related 48-kD JNK phosphorylation while maintaining MPF activity and retarding oocyte degradation. Such findings suggest that a 48-kD JNK may help deactivate MPF and trigger death. Possible mechanisms by which JNK activation either together with, or independently of, protein neosynthesis might stimulate oocyte degradation are discussed.

Keywords

CerebratulusGVBDMPFnemerteanSP600125
Type
Research Article
Information
Zygote , Volume 25 , Issue 6 , December 2017 , pp. 686 - 696
Copyright
Copyright © Cambridge University Press 2017 

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References

Almuedo-Castillo, M., Crespo, X., Seebeck, F., Bartscherer, K., Salo, E. & Adell, T. (2014). JNK controls the onset of mitosis in planarian stem cells and triggers apoptotic death required for regeneration and remodeling. PLoS ONE 6, e1004400.Google Scholar
Amar, S., Glozman, A., Chung, D., Adler, V., Ronai, Z., Friedman, F.K., Robinson, R., Brandt-Rauf, P., Yamaizumi, Z., Pincus, M. R. (1997). Selective inhibition of oncogenic ras-p21 in vivo by agents that block its interaction with jun-N-kinase and jun proteins. Implications for the design of selective chemotherapeutic agents. Cancer Chemother. Pharmacol. 41, 79–85.Google Scholar
Bagowski, C.P. & Ferrell, J. E. (2001). Bistability in the JNK cascade. Curr. Biol. 11, 1176–82.Google Scholar
Bagowski, C.P., Xiong, W. & Ferrell, J. E. (2001). C-Jun N-terminal kinase activation in Xenopus laevis eggs and embryos. J. Biol. Chem. 276, 1459–65.Google Scholar
Bain, J., Plater, L., Elliott, M., Shpiro, N., Hastie, C. J., McLauchlan, H., Klevernic, I, Arthur, J.S.C., Alessi, D.R. & Cohen, P. (2007). The selectivity of protein kinases: a further update. Biochem J. 408, 297–315.Google Scholar
Bogoyevitch, M.A. & Kobe, B. (2006). Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol. Mol. Biol. Rev. 70, 1061–95.Google Scholar
Cano, E., Hazzalin, C.A. & Mahadevan, L.D. (1994). Anisomycin-activated protein kinases p45 and p55 but not mitogen-activated protein kinases ERK-1 and -2 are implicated in the induction of c-fos and c-jun . Mol. Cell. Biol. 14, 7352–62.Google Scholar
Davis, R. J. (2000). Signal transduction by the JNK group of MAP kinases. Cell 103, 239–52.Google Scholar
Deguchi, R., Takeda, N. & Stricker, S. A. (2015). Calcium signals and oocyte maturation in marine invertebrates. Int. J. Dev. Biol. 59, 271–80.CrossRefGoogle ScholarPubMed
Du Pasquier, D., Dupré, A. & Jessus, C. (2011). Unfertilized Xenopus eggs die by Bad-dependent apoptosis under the control of Cdk1 and JNK. PLoS ONE 8, e23672.Google Scholar
Ebeling, S., Labudda, A. & Meinecke, B. (2010). In vitro ageing of porcine oocytes: changes in phosphorylation of the mitogen-activated protein kinase (MAPK) and parthenogenetic activability. Reprod. Dom. Anim. 45, e398–404.Google Scholar
Escalona, J. R. & Stricker, S. A. (2014). Immunoblotting analyses of changes in protein phosphorylations during oocyte maturation in marine nemertean worms. In Methods in Molecular Biology: Developmental Biology of the Sea Urchin and Other Marine Invertebrate Model Systems (eds Carroll, D.J. & Stricker, S.A.). Humana Press, New York.Google Scholar
Fissore, R.A., Kurokawa, M., Knott, J., Zhang, M. & Smyth, J. (2002). Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction 124, 745–54.CrossRefGoogle ScholarPubMed
Fosbrink, M., Aye-Han, N.-N., Cheong, R., Levchenko, A. & Zhang, J. (2010). Visualization of JNK activity dynamics with a genetically encoded fluorescent biosensor. PNAS 107, 5459–64.Google Scholar
Gutierrez, G. J., Tsuji, T., Cross, J.V., Cross, J.V., Davis, R.J., Templeton, D. J., Jiang, W. & Ronai, Z. (2010). JNK-mediated phosphorylation of Cdc25C regulates cell cycle entry and G2/M DNA damage checkpoint. J. Biol. Chem. 285, 14217–28.Google Scholar
Jiang, G.-J., Wang, K., Miao, D.-Q., Guo, L., Huo, Y., Schatten, H. & Schatten, H. (2011). Protein profile changes during porcine oocyte aging and effects of caffeine on protein expression patterns. PLoS ONE 6, ee28996.CrossRefGoogle ScholarPubMed
Kikuchi, K., Izaike, Y., Noguchi, J., Furukawa, T., Daen, F.P., Naito, K. & 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, 325–30.Google Scholar
Kikuchi, K., Naito, K., Noguchi, J., Shimada, A., Kaneko, H., Yamashita, M., Aoki, F., Tojo, H. & Toyoda, Y. (2000). Maturation/M-phase promoting factor: a regulator of aging in porcine oocytes. Biol. Reprod. 63, 715–22.Google Scholar
McGinnis, L. K., Pelech, S. & Kinsey, W. H. (2014). Post-ovulatory aging of oocytes disrupts kinase signaling pathways and lysosome biogenesis. Mol. Reprod. Dev. 81, 928–45.Google Scholar
Messaoud, N.B., Yue, J., Valent, D., Katzarova, I. & Lopez, J. M. (2015). Osmostress-induced apoptosis in Xenopus oocytes: role of stress protein kinases, calpains and Smac/DIABLO. PLoS ONE 10, e0124482.Google Scholar
Miao, Y.-L., Kikuchi, K., Sun, Q.-Y. & Schatten, H. (2009). Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum. Reprod. Update 15, 573–85.Google Scholar
Mood, K., Bong, Y.-S., Lee, H.-S., Ishimura, A & Daar, I. O. (2004). Contribution of JNK, Mek, Mos, and PI-3K signaling to GVBD in Xenopus oocytes. Cell Signal. 16, 631–642.CrossRefGoogle ScholarPubMed
Oksvold, M.P., Pedersen, N.M., Forfang, L. & Smeland, E.B. (2012). Effect of cycloheximide on epidermal growth factor receptor trafficking and signaling. FEBS Lett. 586, 3575–81.Google Scholar
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, 460–71.Google Scholar
Petrova, I, Sedmikova, M., Petr, J., Vodkova, Z., Pytloun, P., Chmelikova, E., Rehak, D., Ctrnacta, A., Rajmon, R., Jilek, F. (2009). The roles of c-Jun N-terminal kinase (JNK) and p38 mitogen-activated protein kinase (p38 MAPK) in aged pig oocytes. J. Reprod. Dev. 55, 75–82.CrossRefGoogle ScholarPubMed
Sadler, K.C., Yuce, O., Hamaratoǧlu, F., Vergé, V., Peaucellier, G. & Picard, A. (2004). MAP kinases regulate unfertilized egg apoptosis and fertilization suppresses death via Ca2+ signaling. Mol. Reprod. Dev. 67, 366–83.Google Scholar
Sasaki, K. & Chiba, K. (2004). Induction of apoptosis in starfish eggs requires spontaneous inactivation of MAPK (extracellular signal-regulated kinase) followed by activation of p38 MAPK. Mol. Biol. Cell 15, 1387–1396.Google Scholar
Sedmikova, M, Petr, J., Dorflerova, A., Nevoral, J., Novotna, B., Krejcova, T., Chmelikova, E. & Tumova, L. (2013). Inhibition of c-Jun N-terminal kinase (JNK) suppresses porcine oocyte ageing in vitro . Czech J. Anim. Sci. 58, 535–45.Google Scholar
Smythe, T. L. & Stricker, S. A. (2005). Germinal vesicle breakdown is not fully dependent on MAPK activation in maturing oocytes of marine nemertean worms. Mol. Reprod. Dev. 70, 91–102.CrossRefGoogle Scholar
Stricker, S. A. (1987). Phylum Nemertea. In Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast (ed. Strathmann, M.). University of Washington Press, Seattle.Google Scholar
Stricker, S.A. (1999). Comparative calcium signaling during fertilization and egg activation in animals. Dev. Biol. 211, 157–76.Google Scholar
Stricker, S. A. (2011). Potential upstream regulators and downstream targets of AMP-activated kinase signaling during oocyte maturation in a marine worm. Reproduction 142, 1–12.Google Scholar
Stricker, S. A. & Smythe, T. L. (2000). Multiple triggers of oocyte maturation in nemertean worms: the roles of calcium and serotonin. J. Exp. Zool. 287, 243–61.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Stricker, S. A. & Smythe, T. L. (2003). Endoplasmic reticulum reorganizations and Ca2+ signaling in maturing and fertilized oocytes of marine protostome worms: the roles of MAPKs and MPF. Development 130, 2867–79.CrossRefGoogle ScholarPubMed
Stricker, S. A. & Smythe, T. L. (2006). Differing mechanisms of cAMP- versus seawater-induced oocyte maturation in marine nemertean worms I. The roles of serine/threonine kinases and phosphatases. Mol. Reprod. Dev. 73, 1578–90.CrossRefGoogle Scholar
Stricker, S.A., Swiderek, L. & Nguyen, T. (2010). Stimulators of AMP-activated kinase inhibit seawater- but not cAMP-induced oocyte maturation in a marine worm: implications for interactions between cAMP and AMPK signaling. Mol. Reprod. Dev. 77, 497–510.Google Scholar
Stricker, S. A., Cline, C. & Goodrich, D. (2013). Oocyte maturation and fertilization in marine nemertean worms: using similar sorts of signaling pathways as in mammals, but often with differing results. Biol. Bull. 224, 137–55.Google Scholar
Stricker, S.A., Beckstrom, B, Mendoza, C., Stanislawski, E. & Wodajo, T. (2016). Oocyte aging in a marine protostome worm: the roles of maturation promoting factor and extracellular signal regulated kinase form of mitogen-activated protein kinase. Dev. Growth Differ. 58, 250–259.Google Scholar
Tang, D.-W., Fang, Y., Liu, Z.-X., Wu, Y., Wang, X.-L., Zhao, S., Han, G.-C. & Zeng, S.-M. (2013). The disturbances of endoplasmic reticulum calcium homeostasis caused by increased intracellular reactive oxygen species contributes to fragmentation in aged porcine oocytes. Biol. Reprod. 89, 1–9.Google Scholar
Tiwari, M., Prasad, S., Tripathi, A., Pandey, A.N., Ali, I., Singh, A.K., Shrivastav, T.G. & Chaube, S.K. (2015). Apoptosis in mammalian oocytes: a review. Apoptosis 20, 1019–25.Google Scholar
Trapphoff, T., Heiligentag, M., Dankert, D., Demond, H., Deutsch, D., Frohlich, T., Arnold, G.J., Grummer, R., Horsthemke, B. & Eichenlaub-Ritter, U. (2015). Postovulatory aging affects dynamics of mRNA, expression and localization of maternal effect proteins, spindle integrity and pericentromeric proteins in mouse oocytes. Hum. Reprod. 31, 133–49.Google Scholar
Wada, T. & Penninger, J.M. (2004). Mitogen-activated protein kinases in apoptosis regulation. Oncogene 23, 2838–49.Google Scholar
Wu, B., Ignotz, G., Currie, B.W. & Yang, X. (1997). Dynamics of maturation-promoting factor and its constituent proteins during in vitro maturation of bovine oocytes. Biol. Reprod. 56, 253–9.CrossRefGoogle ScholarPubMed
Yuce, O. & Sadler, K.C. (2001). Postmeiotic unfertilized starfish eggs die by apoptosis. Dev. Biol. 237, 29–44.Google Scholar
Yue, J. & Lopez, J.M. (2016). JNK does not regulate meiotic progression in Xenopus oocytes. Dev. Biol. 416, 42–51.Google Scholar
Zhang, G.-M., Gu, C.-H., Zhang, Y.-L., Sun, H.-Y., Qian, W.-P., Zhou, Z.-R., Wan, Y.-J., Jia, R.-X., Wang, L.-Z. & Wang, F. (2013). Age-associated changes in gene expression of goat oocytes. Theriogen 80, 328–36.Google Scholar