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Activation of AMP-activated protein kinase may not be involved in AICAR- and metformin-mediated meiotic arrest in bovine denuded and cumulus-enclosed oocytes in vitro

Published online by Cambridge University Press:  23 June 2010

Sylvie Bilodeau-Goeseels ,
Paul L. Panich  and
John P. Kastelic
Sylvie Bilodeau-Goeseels*
Affiliation:
Agriculture and Agri-Food Canada, Lethbridge Research Centre 5403 1st Avenue South, Lethbridge, Alberta, CanadaT1J 4B1.
Paul L. Panich
Affiliation:
Agriculture and Agri-Food Canada, Lethbridge Research Centre 5403 1st Avenue South, Lethbridge, Alberta, CanadaT1J 4B1.
John P. Kastelic
Affiliation:
Agriculture and Agri-Food Canada, Lethbridge Research Centre 5403 1st Avenue South, Lethbridge, Alberta, CanadaT1J 4B1.
*
All correspondence to: Sylvie Bilodeau-Goeseels. Agriculture and Agri-Food Canada, Lethbridge Research Centre 5403 1st Avenue South, Lethbridge, Alberta, CanadaT1J 4B1. Tel: +1 403 317 2290. Fax: +1 403 382 3156. e-mail: [email protected]
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Summary

The adenosine monophosphate-activated protein kinase (AMPK) activators, 5′-aminoimidazole-4-carboxamide 1-β-d-ribofuranoside (AICAR) and metformin (MET), inhibit resumption of meiosis in bovine cumulus-enclosed oocytes (CEO) and denuded oocytes (DO). The objectives of this study were to: (1) examine the effects of AMPK inhibitors on bovine oocyte meiosis in vitro; and (2) determine if AICAR or MET activates oocyte and/or cumulus cell AMPK. The AMPK inhibitor compound C (CC; 0.5, 1, 5, and 10 μM) did not reverse the inhibitory effects of AICAR (1 mM) and MET (2 mM) on bovine oocyte meiosis. Additionally, CC (5 and 10 μM) inhibited meiosis (p < 0.05) in CEO and DO cultured for 7 h. Okadaic acid (1 μM) reversed the inhibitory effect of MET (2 mM) and CC (5 μM; p < 0.05) but not of AICAR (1 mM). Phosphorylation of the alpha subunit of AMPK on Thr172 is required for activation. Based on western blot analysis, AICAR, MET and CC did not affect Thr172 phosphorylation levels in DO and oocytes from complexes (p > 0.05). In cumulus cells, Thr172 phosphorylation decreased after 3 h of culture (p < 0.05), regardless of the presence of AMPK modulators in the culture medium. Higher concentrations of AICAR (2 mM) and MET (10 mM) did not affect Thr172 phosphorylation, but phosphorylation on Ser79 of ACC, a substrate of AMPK, was increased in response to MET (p < 0.05). In conclusion, we inferred that the inhibitory effect of AICAR and MET on bovine oocyte meiosis was probably not mediated through activation of AMPK. Moreover, these compounds probably inhibited meiosis through different pathways.

Keywords

AICA ribosideAMP-activated protein kinaseMeiosisMetforminOocyte
Type
Research Article
Information
Zygote , Volume 19 , Issue 2 , May 2011 , pp. 97 - 106
Copyright
Copyright © Cambridge University Press 2010

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References

Bilodeau-Goeseels, S. (2003). Effects of phosphodiesterase inhibitors on spontaneous nuclear maturation and cAMP concentrations in bovine oocytes. Theriogenology 60, 1679–1690.Google Scholar
Bilodeau-Goeseels, S. (2007). Effects of manipulating the nitric oxide/cyclic GMP pathway on bovine oocyte meiotic resumption in vitro. Theriogenology 68, 693–701.Google Scholar
Bilodeau-Goeseels, S., Sasseville, M., Guillemette, C. & Richard, F.J. (2007). Effects of adenosine monophosphate-activated kinase activators on bovine oocyte nuclear maturation in vitro. Mol. Reprod. Dev. 74, 1021–1034.Google Scholar
Bolster, D.R., Crozier, S.J., Kimball, S.R. & Jefferson, L.S. (2002). AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J. Biol. Chem. 277, 23977–23980.CrossRefGoogle ScholarPubMed
Brunmair, B., Staniek, K., Gras, F., Scharf, N., Althaym, A., Clara, R., Roden, M., Gnaiger, E., Nohl, H., Waldhausl, W. & Furnsinn, C. (2003). Thiazolidinediones, like metformin, inhibit respiratory complex I: a common mechanism contributing to their antidiabetic action? Diabetes 53, 1052–1059.Google Scholar
Bu, S., Xia, G., Tao, Y., Lei, L. & Zhou, B. (2003). Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Mol. Cell. Endocrinol. 207, 21–30.Google Scholar
Chen, J. & Downs, S.M. (2008). AMP-activated protein kinase is involved in hormone-induced mouse oocyte meiotic maturation in vitro. Dev. Biol. 313, 47–57.Google Scholar
Chen, J., Hudson, E., Chi, M.M., Chang, A.S., Moley, K.H., Hardie, D.G. & Downs, S.M. (2006). AMPK regulation of mouse oocyte meiotic resumption in vitro. Dev. Biol. 291, 227–238.CrossRefGoogle ScholarPubMed
Corton, J.M., Gillespie, J.G. & Hardie, D.G. (1994). Role of the AMP-activated protein kinase in the cellular stress response. Curr. Biol. 4, 315–324.Google Scholar
Davies, S.P., Carling, D. & Hardie, D.G. (1989). Tissue distribution of the AMP-activated protein kinase, and lack of activation by cyclic-AMP-dependent protein kinase, studies using a specific and sensitive peptide assay. Eur. J. Biochem. 186, 123–128.Google Scholar
Downs, S.M. (1995). Control of the resumption of meiotic maturation in mammalian oocytes. In: Gametes: The oocyte, Grudzinskas, JG, Yovich, JL, (Eds.), Cambridge Univ. Press, pp. 150–192.Google Scholar
Downs, S.M., Hudson, E.R. & Hardie, D.G. (2002). A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes. Dev. Biol. 245, 200–212.Google Scholar
El-Mir, M.-Y., Nogueira, V., Fontaine, E., Avéret, N., Rigoulet, M. & Leverve, X. (2000). Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J. Biol. Chem. 275, 223–228.Google Scholar
Guigas, B., Bertrand, L., Taleux, N., Foretz, M., Wiernsperger, N., Vertommen, D., Andreelli, F., Viollet, B. & Hue, L. (2006). 5-aminoimidazole-4-carboxamide-1-β-d-ribofuranoside and metformin inhibit hepatic glucose phosphorylation by an AMP-activated protein kinase-independent effect on glucokinase translocation. Diabetes 55, 865–874.CrossRefGoogle ScholarPubMed
Guigas, B., Taleux, N., Foretz, M., Detaille, D., Andreelli, F. & Viollet, B. (2007). AMP-activated protein kinase-independent inhibition of hepatic mitochondrial phosphorylation by AICA riboside. Biochem. J. 404, 499–507.Google Scholar
Hardie, D.G. (2004). The AMP-activated protein kinase pathway – new players upstream and downstream. J. Cell Sci. 117, 5479–5487.CrossRefGoogle ScholarPubMed
Hardie, D.G. & Carling, D. (1997). The AMP-activated protein kinase: An archetypal protein kinase cascade? BioEssays 14, 699–704.CrossRefGoogle Scholar
Horman, S., Browne, G.J., Krause, U., Patel, J.V., Vertommen, D., Bertrand, L., Lavoinne, A., Horner, K., Livera, G., Hinckley, M., Trinh, K., Storm, D. & Conti, M. (2003). Rodent oocytes express an active adenylyl cyclase required for meiotic arrest. Dev. Biol. 258, 385–396.Google Scholar
Hue, L., Proud, C.G., Rider, M.H. (2002). Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr. Biol. 12, 1419–1423.Google Scholar
Kalinowski, R.R., Berlot, C.H., Jones, T.L., Ross, L.F., Jaffe, L.A. & Mehlmann, L.M. (2004). Maintenance of meiotic prophase arrest in vertebrate oocytes by a Gs protein-mediated pathway. Dev. Biol. 267, 1–13.CrossRefGoogle ScholarPubMed
Kalous, J., Kubelka, M., Rimkevicova, Z., Guerrier, P. & Motlik, J. (1993). Okadaic acid accelerates germinal vesicle breakdown and overcomes cycloheximide- and 6-dimethylaminopurine block in cattle and pig oocytes. Dev. Biol. 157, 448–454.CrossRefGoogle ScholarPubMed
López, J.M., Santidrián, AF, Campàs, C. & Gil, J. (2003). 5-aminoimidazole-4-carboxamide riboside induces apoptosis in Jurkat cells, but the AMP-activated protein kinase is not involved. Biochem. J. 370, 1027–1032.Google Scholar
Mayes, M.A. & Sirard, M.A. (2002). Effect of type 3 and type 4 phosphodiesterase inhibitors on the maintenance of bovine oocytes in meiotic arrest. Biol. Reprod. 66, 180–184.Google Scholar
Mayes, M.A., Laforest, M.F., Guillemette, C., Gilchrist, R.B. & Richard, F.J. (2007). Adenosine 5′-monophosphate kinase-activated protein kinase (PRKA) activators delay meiotic resumption in porcine oocytes. Biol. Reprod. 76, 589–597.Google Scholar
Pilon, G., Dallaire, P. & Marette, A. (2004). Inhibition of inducible nitric-oxide synthase by activators of AMP-activated protein kinase: a new mechanism of action of insulin-sensitizing drugs. J. Biol. Chem. 279, 20767–20774.Google Scholar
Shimada, M. & Tarada, T. (2002). Roles of cAMP in regulation of both MAP kinase and p34cdc2 kinase activity during meiotic progression, especially beyond the MI stage. Mol. Reprod. Dev. 62, 124–131.Google Scholar
Sirard, M.A., Florman, H.M., Leibfried-Ruthledge, M.L., Barnes, F.L., Sims, M.L. & First, N.L. (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 40, 1257–1263.Google Scholar
Stefanelli, C., Stanic, I., Bonavita, F., Flamigni, F., Pignatti, C., Guarnieri, C. & Caldarera, C.M. (1998). Inhibition of glucocorticoid-induced apoptosis with 5-aminoimidazole-4-carboxamide ribonucleoside, a cell-permeable activator of AMP-activated protein kinase. Biochem. Res. Comm. 243, 821–826.Google Scholar
Tao, Y., Xie, H., Hong, H., Chen, X., Jang, J. & Xia, G. (2005). Effects of nitric oxide synthase inhibitors on porcine oocyte meiotic maturation. Zygote 13, 1–9.Google Scholar
Thomas, R.E., Armstrong, D.T. & Gilchrist, R.B. (2004). Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3,′5′-monophosphate levels. Biol. Reprod. 70, 548–556.Google Scholar
Tosca, L., Uzbekova, S., Chabrolle, C. & Dupont, J. (2007). Possible role of 5′AMP-activated protein kinase in the metformin-mediated arrest of bovine oocytes at the germinal vesicle stage during in vitro maturation. Biol. Reprod. 77, 368–378.Google Scholar
Tsafriri, A., Chun, S.-Y., Zhang, R., Hsueh, A.J.W. & Conti, M. (1996). Oocyte maturation involves compartmentalization and opposing changes of cAMP concentrations in follicular somatic and germ cells: Studies using selective phosphodiesterase inhibitors. Dev. Biol. 191, 88–102.Google Scholar
Wiersma, A., Hirsch, B., Tsafriri, A., Hanssen, R.G.J.M., Van de Kant, M., Kloosterboer, H.J., Conti, M. & Hsueh, A.J. (1998). Phosphodiesterase 3 inhibitors suppress oocyte maturation and consequent pregnancy without affecting ovulation and cyclicity in rodents. J. Clin. Invest. 102, 532–537.Google Scholar