[en] From C. elegans to mammals (including humans), nutrition and energy metabolism significantly influence reproduction. At the cellular level, some detectors of energy status indicate whether energy reserves are abundant (obesity), or poor (diet restriction). One of these detectors is AMPK (5' AMP-activated protein kinase), a protein kinase activated by ATP deficiency but also by several natural substances such as polyphenols or synthetic molecules like metformin, used in the treatment of insulin resistance. AMPK is expressed in muscle and liver, but also in the ovary and testis. This review focuses on the main effects of AMPK identified in gonadal cells. We describe the role of AMPK in gonadal steroidogenesis, in proliferation and survival of somatic gonadal cells and in the maturation of oocytes or spermatozoa. We discuss also the role of AMPK in germ and somatic cell interactions within the cumulus-oocyte complex and in the blood testis barrier. Finally, the interface in the gonad between AMPK and modification of metabolism is reported and discussion about the role of AMPK on fertility, in regards to the treatment of infertility associated with insulin resistance (male obesity, polycystic ovary syndrome).
Disciplines :
Endocrinology, metabolism & nutrition
Author, co-author :
Bertoldo, Michael J; Discipline of Obstetrics and Gynaecology, School of Women's and Children's
Faure, Mélanie ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Neuroendocrinology ; Unité de Physiologie de la Reproduction et des Comportements, Institut National
Dupont, Joëlle; Unité de Physiologie de la Reproduction et des Comportements, Institut National
Froment, Pascal; Unité de Physiologie de la Reproduction et des Comportements, Institut National
Language :
English
Title :
AMPK: a master energy regulator for gonadal function.
Abdou, H.S., Bergeron, F., and Tremblay, J.J. (2014). A cell-autonomous molecular cascade initiated by AMP-activated protein kinase represses steroidogenesis. Molecular and Cellular Biology 34, 4257-4271.
Akiyama, T., Nagata, M., and Aoki, F. (2006). Inadequate histone deacetylation during oocyte meiosis causes aneauploidy and embryo death in mice. PNAS 103, 7339-7344.
Alesutan, I., Sopjani, M., Munoz, C., Fraser, S., Kemp, B.E., Foller, M., and Lang, F. (2011). Inhibition of connexin 26 by the AMP-activated protein kinase. Journal of Membrane Biology 240, 151-158.
Arrantes-Oliveira, N., Apfeld, J., Dillin, A., and Kenyon, C. (2002). Regulation of life-span by germ-lne stem cells in Caenorhabditis elegans. Science 295, 502-505.
Attia, S.M., Helal, G.K., and Alhaider, A.A. (2009). Assessment of genomic instability in mormal and diabetic rats treated with metformin. Chemico-Biological Interactions 180, 296-304.
Baur, J.A., Pearson, K.J., Price, N.L., Jamieson, H.A., Lerin, C., Prabhu, V.V., Allard, J.S., Lopez-Lluch, G., Lewis, K., Pistell, P.J., Poosala, S., Becker, K.G., Boss, O., Gwinn, D., Wang, M., Ramaswamy, S., Fishbein, K.W., Spencer, R.G., Lakatta, E.G., Le Couteur, D., Shaw, R.J., Navas, P., Puigserver, P., Ingram, D.K., De Cabo, R., and Sinclair, D.A. (2006). Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444, 337-342.
Bendale, D.S., Karpe, P.A., Chhabra, R., Shete, S.P., Shah, H., and Tikoo, K. (2013). 17-β Estradiol prevents cardiovascular dysfunction in post-menopausal metabolic syndrome by involving SIRT1/AMPK/H3 acetylation. British Journal of Pharmacology 170, 779-795.
Bertoldo, M.J., Guibert, E., Faure, M., Rame, C., Foretz, M., Viollet, B., Dupont, J., and Froment, P. (2015). Specific deletion of AMP-activated protein kinase (a1AMPK) in murine oocytes alters junctional protein expression and mitochindrial physiology. PLoS One In press.
Bertoldo, M.J., Guibert, E., Tartarin, P., Guillory, V., and Froment, P. (2014a). Effect of metformin on the fertilizing ability of mouse spermatozoa. Cryobiology 68, 262-268.
Bertoldo, M.J., Locatelli, Y., O'neill, C., and Mermillod, P. (2014b). Impacts of and interactions between environmental stress and epigenetic programming during early embryo development. Reproduction, Fertility and Development doi: 10.1071/RD14049. [Epub ahead of print].
Bertoldo, M.J., Guibert, E., Tartarin, P., Guillou, F., Foretz, M., Viollet, B., Froment, P. (2013). L'AMPK, une protéine impliquée dans les interactions entre les cellules nourricières et les cellules germinales. Annales d'Endocrinologie 74, 266 Doi: 10.1016/j.ando.2013.07.097
Bessone, S., Vidal, F., Le Bouc, Y., Epelbaum, J., Bluet-Pajot, M.T., and Darmon, M. (1999). EMK protein kinase-null mice: dwarfism and hypofertility associated with alterations in the somatotrope and prolactin pathways. Developmental Biology 214, 87-101.
Biggers, J.D., Whittingham, D.G., and Donahue, R.P. (1967). The pattern of energy metabolism in the mouse oocyte and zygote. PNAS 58, 560-567.
Bilodeau-Goeseels, S. (2011). Cows are not mice: the role of cyclic AMP, phosphodiesterases, and adenosine monophosphate-activated protein kinase in the maintenance of meiotic arrest in bovine oocytes Molecular Reproduction and Development 78, 734-743.
Bilodeau-Goeseels, S., Sasseville, M., Guillemette, C., and Richard, F.J. (2007). Effects of adenosine monophosphate-activated kinase activators on bovine oocyte nuclear maturation in vitro. Molecular Reproduction and Development 74, 1021-1034.
Bordone, L., and Guarente, L. (2005). Calorie restriction, SIRT1 and metabolism: understanding longevity. Nat Rev Mol Cell Biol 6, 298-305. doi: nrm1616 [pii] 10.1038/nrm1616.
Brooks, C.L., and Gu, W. (2009). How does SIRT1 affect metabolism, senescence and cancer? Nat Rev Cancer 9, 123-128. doi: nrc2562 [pii] 10.1038/nrc2562.
Brusg, J.M., Ancellin, N., Grondin, P., Guillard, R., Martin, S., Saintillan, Y., and Issandou, M. (2006). Inhibition of lipid synthesis through activation of AMP kinase: an additional mechanism for the hypolipidemic effects of berberine. Journal fo Lipid Research 47, 1281-1288.
Canto, C., and Auwerx, J. (2009). PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr Opin Lipidol 20, 98-105. doi: 10.1097/MOL.0b013e328328d0a4 00041433-200904000-00004 [pii].
Chen, H., Ruan, Y.C., X. W. M., Chen, J., and Chan, H.C. (2012). Regulation of male fertility by CFTR and implications in male infertility. Human Reproduction Update 18, 703-713.
Chen, J., and Downs, S.M. (2008). AMP-activated protein kinase is involved in hormone-induced mouse oocyte meiotic maturation in vitro. Developmental Biology 313, 47-57.
Chen, J., Hudson, E., Chi, M.M., Chang, A.S., Moley, K.H., Hardie, D.G., and Downs, S.M. (2006). AMPK regulation of mouse oocyte meiotic resumption in vitro. Developmental Biology 291, 227-238.
Choi, K.M., Lee, Y.S., Kim, W., Kim, S.J., Shin, K.O., Yu, J.Y., Lee, M.K., Lee, Y.M., Hong, J.T., Yun, Y.P., and Yoo, H.S. (2014). Sulforaphane attenuates obesity by inhibiting adipogenesis and activating the AMPK pathway in obese mice. Journal of Nutritional Biochemistry 25, 201-207.
Cordova, A., Strobel, P., Vallejo, A., Valenzuela, P., Ulloa, O., Burgoa, R.A., Menarim, B., Rodriguez-Gil, J.E., Ratto, M., and Ramirez-Reveco, A. (2014). Use of hypometabolic TRIS extenders and high cooling rate refrigeration for cryopreservation of stallion sperm: Presence and sensitivity of 5' AMP-activated protein kinase (AMPK). Cryobiology 69, 473-481.
Coussens, M., Maresh, J.G., Yanagimachi, R., Maeda, G., and Allsopp, R. (2008). Sirt1 deficiency attenuates spermatogenesis and germ cell function. Plos One 3, e1571.
Creighton, J., Jian, M., Sayner, S., Alexeyev, M., and Insel, P.A. (2011). Adenosine monophosphate activated kinase alpha1 promotes endothelial barrier repair. FASEB Journal 25, 3356-3365.
Dhahbi, J.M., Mote, P.L., Fahy, G.M., and Spindler, S.R. (2005). Identification of potential caloric restriction mimetics by mircroarray profiling. Physiological Genomics 23, 343-350.
Downs, S.M. (2011). Mouse versus rat: Profound differences in meiotic regulation at the level of the isolated oocyte. Molecular Reproduction and Development 78, 778-794.
Downs, S.M., and Chen, J. (2006). Induction of meiotic maturation in mouse oocytes by adenosine analogs. Molecular Reproduction and Development 73, 1159-1168.
Downs, S.M., Hudson, E.R., and Hardie, D.G. (2002). A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes. Developmental Biology 245, 200-212.
Downs, S.M., Humpherson, P.G., Martin, K.L., and Leese, H.J. (1996). Glucose utilization during gonadotropin-induced meiotic maturation in cumulus-cell enclosed mouse oocytes. Molecular Reproduction and Development 44, 121-131.
Downs, S.M., and Mastropolo, A.M. (1994). The participation of energy substrates in the control og meiotic maturation in murine oocytes. Developmental Biology 162, 154-168.
Downs, S.M., Ya, R., and Davis, C.C. (2010). Role of AMPK throughout meiotic maturation in the mouse oocyte: evidence for promotion of polar body formation and suppression of premature activation. Molecular Reproduction and Development 77, 888-899.
Drummond-Barbosa, D., and Spradling, A.C. (2001). Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Developmental Biology 231, 265-278.
Dupont, J., Reverchon, M., Cloix, L., Froment, P., and Rame, C. (2012). Involvement of adipokines, AMPK, PI3K and the PPAR signaling pathways in ovarian follicle development and cancer. Int J Dev Biol 56, 959-967. doi: 120134jd [pii] 10.1387/ijdb.120134jd.
El-Mir, M.Y., Nogueira, V., Fontaine, E., Averet, N., Rigoulet, M., and Leverve, X. (2000). Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. Journal of Biological Chemistry 275, 223-228.
Faubert, B., Boily, G., Izreig, S., Griss, T., Samborska, B., Dong, Z., Dupuy, F., Chambers, C., Fuerth, B.J., Viollet, B., Mamer, O.A., Avizonis, D., Deberardinis, R.J., Siegel, P.M., and Jones, R.G. (2013). AMPK is a negative regulator of the Warburg effect and suppresses tumor growth in vivo. Cell Metabolism 17, 113-124.
Fryer, L.G., Parbu-Patel, A., and Carling, D. (2002). The Anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways. Journal of Biological Chemistry 277, 25226-25232.
Fukuyama, M., Sakuma, K., Park, R., Kasuga, H., Nagaya, R., Atsumi, Y., Shimomura, Y., Takahashi, S., Kajiho, H., Rougvie, A., Kontani, K., and Katada, T. (2012). C. elegans AMPKs promote survival and arrest germline development during nutrient stress. Biology Open 1, 929-936.
Fulco, M., Cen, Y., Zhao, P., Hoffman, E.P., Mcburney, M.W., Sauve, A.A., and Sartorelli, V. (2008). Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Developmental Cell 14, 661-673.
Galardo, M.N., Riera, M.F., Pellizzari, E.H., Cigorraga, S.B., and Meroni, S.B. (2007). The AMP activated protein kinase activator, 5-aminoimidazole-4-carboxamide-1-b-D-ribonucleoside, regulates lactate production in rat Sertoli cells. Journal of Molecular Endocrinology 39, 279-288.
Galardo, M.N., Riera, M.F., Pellizzari, E.H., Sobarzo, C., Scarcelli, R., Denduchis, B., Lustig, L., Cigorraga, S.B., and Meroni, S.B. (2010). Adenosine regulates Sertoli cell function by activating AMPK. Mol Cell Endocrinol 330, 49-58.
Garcez, M.E., Dos Santos Branco, C., Lara, L.V., Pasqualotto, F.F., and Salvador, M. (2010). Effects of resveratrol supplementation on cryopreservation medium of human semen Fertility and Sterility 94, 2118-2121.
Gems, D., and Partridge, L. (2008). Stress-response hormesis and aging: "that which does not kill us makes us stronger". Cell Metab 7, 200-203. doi: 10.1016/j.cmet.2008.01.001.
Gharibi, S.H., Hajian, M., Ostadhosseini, S., Forouzanfar, M., and Nasr-Esfahani, M.H. (2013). Effect of phosphodiesterase type 3 inhibitor on nuclear maturation and in vitro development of ovine oocytes. Theriogenology 80, 302-312.
Ghillebert, R., Swinnen, E., Wen, J., Vandesteene, L., Ramon, M., Norga, K., Rolland, F., and Winderickx, J. (2011). The AMPK/SNF1/SnRK1 fuel gauge and energy regulator: structure, function and regulation. FEBS J 278, 3978-3990. doi: 10.1111/j.1742-4658.2011.08315.x.
Gilchrist, R.B. (2011). Recent insights into oocyte-follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reproduction, Fertility and Development 23, 23-31.
Gilchrist, R.B., Ritter, L.J., and Arsmstrong, D.T. (2004). Oocyte-somatic cell interactions during follicle development in mammals. Animal Reproduction Science 82-83, 431-446.
Guévelou, E., Huvet, A., Galindo-Sanchez, C.E., Milan, M., Quillien, V., Daniel, J.-Y., Quéré, C., Boudry, P., and Corporeau, C. (2013). Sex-specific regulation of AMP-activated protein kinase (AMP) in the Pacific Oyster Crassostrea gigas. Biology of Reproduction 89, 1-15.
Haigis, M.C., and Sinclair, D.A. (2010). Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol 5, 253-295. doi: 10.1146/annurev.pathol.4.110807.092250.
Ham, S., Meachem, S.J., Choong, C.S., Charles, A.K., Baynam, G.S., Jones, T.W., Samarajeewa, N.U., Simpson, E.R., and Brown, K.A. (2013). Overexpression of aromatase associated with loss of heterozygosity of the STK11 gene accounts for prepubertal gynecomastia in boys with Peutz- Jeghers syndrome. Journal of Clinical Endocrinology and Metabolism 98, E1979-1987.
Hardie, D.G. (2011). AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes and Development 25, 1895-1908.
Hardie, D.G. (2015). AMPK: positive and negative regulation, and its role in whole-body energy homeostasis. Curr Opin Cell Biol 33, 1-7. doi: S0955-0674(14)00106-9 [pii] 10.1016/j.ceb.2014.09.004.
Hardie, D.G., Scott, J.W., Pan, D.A., and Hudson, E.R. (2003). Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett 546, 113-120. doi: S001457930300560X [pii].
Harper, K.M., and Brackett, B.G. (1993). Bovine blastocyst development after in vitro maturation in a defined medium with epidermal growth factor and low concentrations of gonadotropins. Biol Reprod 48, 409-416.
Hawley, S.A., Pan, D.A., Musatrd, K.J., Ross, L., Bain, J., Edelman, A.M., Frenguelli, B.G., and Hardie, D.G. (2005). Calmodulin-dependent protein kinase kinase-beta is an alternative upstrream kinase for AMP-activated protein kinase. Cell Metabolism 2, 9-19.
Hernandez, M., Shao, Q., Yang, X.J., Luh, S.P., Kandouz, M., Batist, G., Laird, D.W., and Alaoui-Jamali, M.A. (2006). A histone deacetylation-dependent mechanism for transcriptional repression of the gap junction gene cx43 in prostate cancer cells. Prostate 66, 1151-1161.
Hirsch, A., Hahn, D., Kempna, P., Hofer, G., Mullis, P.E., Nuoffer, J.M., and Fluck, C.E. (2012). Role of AMP-activated protein kinase on steroid hormone biosynthesis in adrenal NCI-H295R cells. PLoS One 7, e30956.
Hormon, S., Browne, G., Krause, U., Patel, J., Vertommen, D., Bertrand, L., Lavoinne, A., Hue, L., Proud, C., and Rider, M. (2002). Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Current Biology 12, 1419-1423.
Hurtado De Llera, A., Martin-Hidago, D., Gil, M.C., Garcia-Marin, L.J., and Bragado, M.J. (2012a). AMP-activated kinase AMPK is expressed in boar spermatozoa and regulates motility. PLoS One 7, e38840.
Hurtado De Llera, A., Martin-Hidago, D., Gil, M.C., Garcia-Marin, L.J., and Bragado, M.J. (2012b). The AMPK activator metformin inhibits one of the main functions of boar spermatozoa, motility. FEBS Journal 279 Suppl. 1, 52-576.
Hurtado De Llera, A., Martin-Hidago, D., Rodriguez-Gil, J.E., Gil, M.C., Garcia-Marin, L.J., and Bragado, M.J. (2013). AMP-activated kinase, AMPK, is involved in the maintenance of plasma membrane organization in boar. Biochimica et Biophysica Acta 1928, 2143-2151.
Hurtado De Llera, A., Martin-Hidalgo, D., Gil, M.C., Garcia-Marin, L.J., and Bragado, M.J. (2015). AMPK up-activation reduces motility and regulates other functions of boar spermatozoa. Mol Hum Reprod 21, 31-45. doi: gau091 [pii] 10.1093/molehr/gau091.
Jaleel, M., Mcbride, A., Lizcano, J.M., Deak, M., Toth, R., Morrice, N.A., and Alessi, D.R. (2005). Identification of the sucrose non-fermenting realted kinase SNRK, as a novel LKB1 substrate. FEBS Letters 579, 1417-1423.
Joseph, B.K., Liu, H.Y., Francisco, J., Pandya, D., Donigan, M., Gallo-Ebert, C., Giordano, C., Bata, A., and Nickels, J.T., Jr. (2015). Inhibition of AMP Kinase by the Protein Phosphatase 2A Heterotrimer, PP2APpp2r2d. J Biol Chem 290, 10588-10598. doi: M114.626259 [pii] 10.1074/jbc.M114.626259.
Kalender, A., Selvaraj, A., Gulati, P., Brule, S., Viollet, B., Kemp, B.E., Bardeesy, N., Dennis, P., Schlager, J.J., Marette, A., Kozma, S.C., and Thomas, G. (2010). Metformin, independent of AMPK, inhibits mTORC1 in a rag GTPase-dependent manner. Cell Metabolism 11, 390-401.
Kayampilly, P.P., and Menon, K.M. (2009). Follicle-stimulating hormone inhibits adenosine 5'- monophosphate-activated protein kinase activation and promotes cell proliferation of primary granulosa cells in culture through an Akt-dependent pathway. Endocrinology 150, 929-935. doi: en.2008-1032 [pii] 10.1210/en.2008-1032.
Kayampilly, P.P., and Menon, K.M. (2012). AMPK activation by dihydrotestosterone reduces FSH stimulated cell proliferation in rat granulosa cells by inhibiting ERK signaling pathway. Endocrinology 153, 2831-2838.
Kerr, G.E., Young, J.C., Horvay, K., Abud, H.E., and Loveland, K.L. (2013). Regulated Wnt/Beta-catenin signaling sustains adult spermatogenesis in mice. Biology of Reproduction Epub ahead of print.
Kierszenbaum, A.L., and Tres, L.L. (2004). The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head. Arch Histol Cytol 67, 271-284.
Kleymenova, E., Swanson, C., Boekelheide, K., and Gaido, K.W. (2005). Exposure in utero to di(n-butyl) phthalate alters the vimentin cytoskeleton of fetal rat Sertoli cells and disrupts Sertoli cell-gonocyte contact. Biology of Reproduction 73, 482-490.
Kojima, Y., Miyoshi, H., Clevers, H.C., Oshima, M., Aoki, M., and Taketo, M.M. (2007). Suppression of tubulin polymerization by the LKB1-microtubule-associated protein/microtubule affinity regulating kinase signaling. Journal of Biological Chemistry 282, 23532-23540.
Kopera, I.A., Bilinska, B., Cheng, C.Y., and Mruk, D.D. (2010). Sertoli-germ cell junctions in the testis: a review of recent data. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365, 1593-15605.
La Marca, A., Eqbe, T.O., Morqante, G., Paglia, T., Cianci, A., and De Leo, V. (2000). Metformin treatment reduces ovarian cytochrome P-450c17alpha response to human chorionic gonadotrophin in women with insulin resistance-related polycystic ovary syndrome. Human Reproduction 15, 21-23.
Lafever, L., and Drummond-Barbosa, D. (2005). Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila. Science 309, 1071-1073.
Lafever, L., Feokitistov, A., Hsu, H.J., and Drummond-Barbosa, D. (2010). Specific roles of target of rapmycin in the control of stem cells and their progeny in the Drosophila ovary. Development 137, 2117-2126.
Larosa, C., and Downs, S.M. (2007). Meiotic inductionb by heat stress in mouse oocytes: Involvement of AMP-activated protein kinase and MAPK family members. Biology of Reproduction 76, 476-486.
Lee, H., Cho, J.S., Lambacher, N., Lee, J., Lee, S.J., Lee, T.H., Gartner, A., and Koo, H.S. (2008). The Caenorhabditis elegans AMP-activated protein kinase AAK-2 is phosphorylated by LKB1 and is required for resistance to oxidative stress and for normal motility and foraging behavior. J Biol Chem 283, 14988-14993. doi: M709115200 [pii] 10.1074/jbc.M709115200.
Lee, N.P.Y., Mruk, D., Wong, C., and Cheng, C.Y. (2005). Regulation of Sertoli-Germ cell adherens junction dynamics in the testis via the nitric oxide synthase (NOS)/cGMP/protein kinase G (PRKG)/ β-catenin (CATNB) signaling pathway: An in vitro and in vivo study. Biology of Reproduction 73, 458-471.
Leese, H.J., and Barton, A.M. (1984). Pyruvate and glucose uptake by mouse ova and preimplantation embryos. Journal of Reproduction and Fertility 72, 9-13.
Lewis, S.E., Boyle, P.M., Mckinney, K.A., Young, I.S., and Thompson, W. (1995). Total antioxidant capacity of seminal plasma is different in fertile and infertile men. Fertility and Sterility 64, 868-870.
Li, R., and Albertini, D.F. (2013). The road to maturation: Somatic cell interaction and self organization of the mammalian oocyte. Nature Reviews Molecular Cell Biology 14, 141-152.
Liang, H., Yoo, S.E., Na, R., Walter, C.A., Richardson, A., and Ran, Q. (2009). Short form glutathione peroxidase 4 is the essential isoform required for survival and somatic mitochondrial functions. J Biol Chem 284, 30836-30844.
Lonergan, P., Carolan, C., Van Langendonckt, A., Donnay, I., Khatir, H., and Mermillod, P. (1996). Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro. Biol Reprod 54, 1420-1429.
Lu, J., Wu, D.M., Zheng, Y.L., Hu, B., Zhang, Z.F., Shan, Q., Zheng, Z.H., Liu, C.M., and Wang, Y.J. (2010). Quercetin activates AMP-activated protein kinase by reducing PP2C expression protecting old mouse brain against high cholesterol-induced neurotoxicity. J Pathol 222, 199-212. doi: 10.1002/path.2754.
Lui, W.Y., and Lee, W.M. (2005). cAMP perturbs inter- Sertoli tight junction permeability barrier in vitro via its effect on proteasome-sensitive ubiquitination of occludin. Journal of Cellular Physiology 203, 564-572.
Macaulay, A.D., Gilbert, I., Caballero, J., Barreto, R., Fournier, E., Tossou, P., Sirard, M.A., Clarke, H.J., Khandjian, E.W., Richard, F.J., Hyttel, P., and Robert, C. (2014). The gametic synapse: RNA transfer to the bovine oocyte. Biolgy of Reproduction 91, 90.
Machell, N.H., and Farookhi, R. (2003). E- and N-cadherin expression and distribution during luteinization in the rat ovary. Reproduction 125, 791-800.
Martin-Hidago, D., Hurtado De Llera, A., Yeste, M., Cruz Gil, M., Bragado, M.J., and Garcia-Marin, L.J. (2013). Adenosine monophosphate-activated kinase, AMPK, is involved in the maintenance of the quality of extended boar semen during long-term storage. Theriogenology Epub ahead of print.
Martin-Montalvo, A., Mercken, E.M., Mitchell, S.J., Palacios, H.H., Mote, P.L., Scheibye-Knudsen, M., Gomes, A.P., Ward, T.M., Minor, R.K., Blouin, M.J., Schwab, M., Pollak, M., Zhang, Y., Yu, Y., Becker, K.G., Bohr, V.A., Ingram, D.K., Sinclair, D.A., Wolf, N.S., Spindler, S.R., and Bernier, M., De Cabo, R. (2013). Metformin improves healthspan and lifespan in mice. Nature Communications 4, 2192.
Mayes, M.A., Laforest, M.F., Guillemette, C., Gilchrist, R.B., and Richard, F.J. (2007). Adenosine 5'- monophosphate kinase-activated protein kinase (PRKA) activators delay meiotic resumption in porcine oocytes. Biology of Reproduction 76, 589-597.
Mueller, S., Rosenquist, T.A., Takai, Y., Bronson, R.A., and Wimmer, E. (2003). Loss of nectin-2 at Sertoli-spermatid junctions leads to male infertility and correlates with severe spermatozoan head and midpiece malformation, impaired binding to the zona pellucida, and oocyte penetration. Biol Reprod 69, 1330-1340.
Nakada, K., Sato, A., Yoshida, K., Morita, T., Tanaka, H., Inoue, S., Yonekawa, H., and Hayashi, J. (2006). Mitochondria-related male infertility. Proc Natl Acad Sci U S A 103, 15148-15153.
Narala, S.R., Allsopp, R.C., Wells, T.B., Zhang, G., Prasad, P., Coussens, M.J., Rossi, D.J., Weissman, I.L., and Vaziri, H. (2008). SIRT1 acts as a nutrient-sensitive growth suppressor and its loss is associated with increased AMPK and telomerase activity. Molecular Biology of the Cell 19, 1210-1219.
Nelson, L.E., Valentine, R.J., Cacicedo, J.M., Gauthier, M.-S., Ido, Y., and Ruderman, N.B. (2012). A novel inverse relationship between metformin-triggered AMPK-SIRT1 signaling and p53 protein abundance in high glucose-exposed HepG2 cells. American Journal of Physiology Cell Physiology 303, C4-C13.
Nguyen, T.M.D., Alves, S., Grasseau, I., Metayer-Coustard, S., Praud, C., Froment, P., and Blesbois, E. (2014). Central role of 5'-AMP-activated protein kinase in cheicken sperm functions. Biology of Reproduction 91, 1-15.
Ogawa, T., Hayashi, T., Tokunou, M., Nakachi, K., Trosko, J.E., Chang, C.C., and Yorioka, N. (2005). Suberoylanilide hydroxamic acid enhances gap junctional intercellular communication via acetylation of histone containing connexin 43 gene locus. Cancer Research 65, 9771-9778.
Onken, B., and Driscoll, M. (2010). Metformin induces a dietary restriction-like state and oxidative stress response to extend C. elegans healthspan via AMPK, LKB1, and SKN-1. PLoS One 5, e8758.
Owen, M.R., Doran, E., and Halestrap, A.P. (2000). Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochemical Journal 348, 607-614.
Pellatt, L.J., Rice, S., and Mason, H.D. (2011). Phosphorylation and activation of AMP-activated protein kinase (AMPK) by metformin in the human ovary requires insulin. Endocrinology 152, 1112-1118. doi: en.2009-1429 [pii] 10.1210/en.2009-1429.
Pelliccione, F., Micillo, A., Cordeschi, G., D'angeli, A., Necozione, S., Gandini, L., Lenzi, A., Francavilla, F., and Francavilla, S. (2011). Altered ultrastructure of mitochondrial membranes is strongly associated with unexplained asthenozoospermia. Fertility and Sterility 95, 641-646.
Peluso, J.J. (2006). N-cadherin mediated cell contact inhibits germinal vesicle brakdown in mouse oocytes maintained in vitro. Reproduction 131, 429-437.
Perez, G.I., Trbovich, A.M., Gosden, R.G., and Tilly, J.L. (2000). Mitochondria and the death of oocytes. Nature 403, 500-501.
Pikiou, O., Vasilaki, A., Leondaritis, G., Vamvakopoulos, N., and Messinis, I.E. (2015). Effects of metformin of fertilisation of bovine oocytes and early embryo development: possible involvement of AMPK3-mediated TSC2 activation. Zygote 23, 58-67.
Proud, C.G. (2004). Role of mTOR signalling in the control of translation initiation and elongation of nutrients. Current Topics in Microbiology and Immunology 279, 215-244.
Ratchford, A.M., Chang, A.S., Chi, M.M.-Y., Sheridan, R., and Moley, K.H. (2007). Maternal diabetes adversely affects AMP-activated protein kinase activity and cellular metabolism in murine oocytes. American Journal of Physiology, Endocrinology and Metabolism 293, E1198-E1206.
Ratchford, A.M., Esguerra, C.R., and Moley, K.H. (2008). Decreased oocyte-granulosa cell gap junction communication and connexin expression in a Type 1 diabetic mouse model. Molecular Endocrinology 22, 2643-2654.
Rice, S., Elia, S., Jawad, Z., Pellatt, L., and Mason, H.D. (2913). Metformin inhibits follicle-stimulating hormone (FSH) action in human granulosa cell: Relevance to polycystic ovary syndrome. Journal of Clinical Endocrinology and Metabolism 98, E1491-E1500.
Richardson, M.C., Ingamells, S., Simonis, C.D., Cameron, I.T., Sreekumar, R., Vijendren, A., Sellahewa, L., Coakley, S., and Byrne, C.D. (2009). Stimulation of lactate production in human granulosa cells by metformin and potential involvement of adenosine 5' monophosphate-activated protein kinase. Journal of Clinical Endocrinology and Metabolism 94, 670-677.
Rider, M.H., Hussain, N., Horman, S., Dilworth, S.M., and Storey, K.B. (2006). Stress-induced activation of the AMP-activated protein kinase in the freeze tolerant frog Rana sylvatica. Cryobiology 53, 297-309.
Riera, M.F., Regueira, M., Galardo, M.N., Pellizzari, E.H., Meroni, S.B., and Cigorraga, S.B. (2012). Signal transduction pathways in FSH regulation of rat Sertoli cell proliferation American Journal of Physiology, Endocrinology and Metabolism 302, E914-923.
Ritter, L.J., Sugimura, S., and Gilchrist, R.B. (2015). Oocyte induction of EGF responsiveness in somatic cells is associated with the acquisition of porcine oocyte developmental competence. Endocrinology, en20141884. doi: 10.1210/en.2014-1884.
Roberts, R., Franks, S., and Hardy, K. (2002). Culture environment modulates maturation and metabolism of human oocytes Human Reproduction 17, 2950-2956.
Rufas, O., Fisch, B., Ziv, S., and Shalgi, R. (2000). Expression of cadherin adhesion molecules on human gametes. Molecular Human Reproduction 6, 163-169.
Saether, T., Tran, T.N., Rootwelt, H., Christophersen, B.O., and Haugen, T.B. (2003). Expression and regulation of delta5-desaturase, delta6-desaturase, stearoyl-coenzyme A (CoA) desaturase 1, and stearoyl-CoA desaturase 2 in rat testis. Biology of Reproduction 69, 117-124.
Santiquet, N., Sasseville, M., Laforest, M., Guillemette, C., Gilchrist, R.B., and Richard, F.J. (2014). Activation of 5' adenosine monophosphate-activated protein kinase blocks cumulus cell expansion through inhibition of protein synthesis during in vitro maturation in swine. Biology of Reproduction 91, 1-12.
Schneider, M., Forster, H., Boersma, A., Seiler, A., Wehnes, H., Sinowatz, F., Neumuller, C., Deutsch, M.J., Walch, A., Hrabe De Angelis, M., Wurst, W., Ursini, F., Roveri, A., Maleszewski, M., Maiorino, M., and Conrad, M. (2009). Mitochondrial glutathione peroxidase 4 disruption causes male infertility. Faseb J 23, 3233-3242.
Scobey, M.J., Bertera, S., Somers, J.P., Watkins, S.C., Zeleznik, A.J., and Walker, W.H. (2001). Delivery of a cylic adenosine 3',5'-monophosphate response element-binding protein (CREB) mutant to seminiferous tubules results in impaired spermatogenesis. Endocrinology 142, 948-954.
Selva, D.M., Hirsch-Reinshagen, V., Burgess, B., Zhou, S., Chan, J., Mcisaac, S., Hayden, M.R., Hammond, G.L., Vogl, A.W., and Wellington, C.L. (2004). The ATP-binding cassette transporter 1 mediates lipid efflux from Sertoli cells and influences male fertility. J Lipid Res 45, 1040-1050. doi: 10.1194/jlr.M400007-JLR200.
Shyh-Chang, N., Daley, G.Q., and Cantley, L.C. (2013). Stem cell metabolism in tissue development and aging. Development 140, 2535-2547.
Simon, A.M., Goodenough, D.A., Li, E., and Paul, D.L. (1997). Female fertility in mice lacking connexin 37. Nature 385, 525-529.
Slack, C., Foley, A., and Partridge, L. (2012). Activation of AMPK by the putative dietary restriction mimetic metformin is insufficient to extend lifespan in Drosophila. PLoS One 7, e47699.
Stricker, S.A. (2011). Potential upstream regulators and downstream targets of AMP-activated kinase signaling during oocyte maturation in a marine worm. Reproduction 142, 29-39.
Stricker, S.A., Cline, C., and 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. The Biological Bulletin 224, 137-155.
Stricker, S.A., Swiderek, L., and Nguyen, T. (2010). Stimulators of AMP-activated kinase (AMPK) inhibit seawater-but not cAMP-induced oocyte maturation in a marine worm: Implications for interactions between cAMP and AMPK signaling. Molecular Reproduction and Development 77, 497-510.
Surace, E.I., Strickland, A., Hess, R.A., Gutmann, D.H., and Naughton, C.K. (2006). Tslc1 (nectin-like molecule-2) is essential for spermatozoa motility and male fertility. J Androl 27, 816-825.
Sutton, M.L., Cetica, P.D., Beconi, M.T., Kind, M.L., Gilchrist, R.B., and Thompson, J.G. (2003a). Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction 126, 27-43.
Sutton, M.L., Gilchrist, R.B., and Thompson, J.G. (2003b). Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity. Human Reproduction Update.
Svechnikov, K., Spatafora, C., Svechnikova, I., Tringali, C., and Soder, O. (2009). Effects of resveratrol analogs on steroidogenesis and mitochondrial function in rat Leydig cells in vitro Journal of Applied Toxicology 29, 673-680.
Tanwar, P.S., Kaneko-Tarui, T., Zhang, L., Rani, P., Taketo, M.M., and Teixeira, J. (2010). Constitutive WNT/Beta-catenin signaling in murine Sertoli cells disrupts their differentiation and ability to support spermatogenesis. Biology of Reproduction 82, 422-432.
Tanwar, P.S., Kaneko-Tarui, T., Zhang, L., and Teixeira, J.M. (2012). Altered LKB1/AMPK/TSC1/TSC2/mTOR signaling causes disruption of Sertoli cell polarity and spermatogenesis. Human Molecular Genetics 21, 4394-4405.
Tartarin, P., Guibert, E., Touré, A., Ouiste, C., Leclerc, J., Sanz, N., Brière, S., Dacheux, J.-L., Delaleu, B., Mcneilly, J.R., Mcneilly, A.S., Brillard, J.-P., Dupont, J., Foretz, M., Viollet, B., and Froment, P. (2012a). Inactivation of AMPKa1 induces asthenozoospermia and alters spermatozoa morphology. Endocrinology 153, 3468-3481.
Tartarin, P., Moison, D., Guibert, E., Dupont, J., Habert, R., Rouiller-Fabre, V., Frydman, N., Pozzi, S., Frydman, R., Lecureuil, C., and Froment, P. (2012b). Metformin exposure affects human and mouse fetal testicular cells. Human Reproduction 27, 3304-3314.
Thirunavukkarasu, M., Penumathsa, S., Juhasz, B., Zhan, L., Bagchi, M., Yasmin, T., Shara, M.A., Thatte, H.S., Bagchi, D., and Maulik, N. (2006). Enhanced cardiovascular function and energy level by a novel chromium (III)-supplement. Biofactors 2006, 53-67.
Thomas, R.E., Armstrong, D.T., and 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'-monophosophate levels. Biology of Reproduction 70, 548-556.
Thouas, G.A., Trounson, A.O., Wolvetang, E.J., and Jones, G.M. (2004). Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biology of Reproduction 71, 1936-1942.
Tosca, L., Chabrolle, C., Uzbekova, S., and Dupont, J. (2007a). Effect of metformin on bovine granulosa cell steroidogenesis: Possible involvement of adenosine 5' monophosphate activated protein kinase (AMPK). Biology of Reproduction 76, 368-378.
Tosca, L., Crochet, S., Ferré, P., Foufelle, F., Tesseraud, S., and Dupont, J. (2006a). AMP-activated protein kinase activation modulates progesterone secretion in granulosa cells from hen preovulatory follicles. Journal of Endocrinology 190, 85-97.
Tosca, L., Froment, P., Solnais, P., Foufelle, F., and Dupont, J. (2005). Adenosine 5'-monophosphate activated protein kinase regulates progesterone secretion in rat granulosa cells. Endocrinology 146, 4500-4513.
Tosca, L., Rame, C., Chabrolle, C., Tesseraud, S., and Dupont, J. (2010). Metformin decreases IGF1- induced cel proliferation and protein synthesis through AMP-activated protein kinase in cultured bovine granulosa cells Reproduction 139, 409-418.
Tosca, L., Solnais, P., Ferre, P., Foufelle, F., and Dupont, J. (2006b). Metformin-induced stimulation of adenosine 5' monophosphate-activated protein kinase (PRKA) impairs progesterone secretion in rat granulosa cells. Biol Reprod 75, 342-351. doi: biolreprod.106.050831 [pii] 10.1095/biolreprod.106.050831.
Tosca, L., Uzbekova, S., Chabrolle, C., and Dupont, J. (2007b). 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 Biology of Reproduction 77, 452-465.
Towler, M.C., Fogarty, S., Hawley, S.A., Pan, D.A., Martin, D.M., Morrice, N.A., Mccarthy, A., Galardo, M.N., Meroni, S.B., Cigorraga, S.B., Ashworth, A., Sakamoto, K., and Hardie, D.G. (2008). A novel short splice variant of the tumour suppressor LKB1 is required for spermiogenesis. Biochem J 416, 1-14.
Ulbright, T.M., Amin, M.B., and Young, R.H. (2007). Intratubular large cell hyalinizing sertoli cell neoplasia of the testis: a report of 8 cases of a distinctive lesion of the Peutz-Jeghers syndrome. American Journal of Surgical Pathology 31, 827-835.
Van Blerkom, J. (2004). Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic ergulation and developmental competence. Reproduction 128, 269-280.
Vaquero, A., Scher, M., Lee, D., Erdjument-Bromage, H., Tempst, P., and Reinberg, D. (2004a). Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin. Molecular Cell 16, 93-105.
Vaquero, A., Scher, M., Lee, D., Erdument-Bromage, H., Tempst, P., and Reinberg, D. (2004b). Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin. Molecular Cell 16, 93-105.
Vasangkar, D., and Downs, S.M. (2013). A requirement for fatty acid oxidation in the hormone induced meiotic maturation of mouse oocytes. Biology of Reproduction 89, 43. doi: 10.1095/biolreprod.1113.109058. Print 102013 Aug.
Wakeling, L.A., Ions, L.J., and Ford, D. (2009). Could Sirt1-mediated epigenetic effects contribute to the longevity response to dietary restriction and be mimicked by other dietary interventions? Age 31, 327-341.
Wang, Q., Ratchford, A.M., Chi, M.M.-Y., Schoeller, E., Frolova, A., Schedl, T., and Moley, K.H. (2009). Maternal diabetes causes mitochondrial dysfunction and meiotic defects in murine oocytes Molecular Endocrinology 23 1603-1612.
Winterhager, E., and Kidder, G.M. (2015). Gap junction connexins in female reproductive organs: implications for women's reproductive health Human Reproduction Update epub ahead of print, doi:10.1093/humupd/dmv1007.
Woods, A., Johnstone, S.R., Dickerson, K., Leiper, F.C., Fryer, L.G., Neumann, D., Schlattner, U., Wallimann, T., Calson, M., and Carling, D. (2003). LKB1 is the upstream kinase in the AMP activated protein kinase cascade. Current Biology 13, 2004-2008.
Ya, R., and Downs, S.M. (2014). Perturbing microtubule integrity blocks AMP-activated protein kinase-induced meiotic resumption in cultured mouse oocytes. Zygote 22, 91-102.
Zhou, G., Myers, R., Li. Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., Musi, N., Hirshman, M.F., Goodyear, L.J., and Moller, D.E. (2001). Role of AMP-activated protein kinase in mechanism of metformin action. Journal of Clinical Investigation 108, 1167- 1174.
Ziv, S., Rufas, O., and Shalgi, R. (2002). Cadherin expression during gamete maturation and fertilzation in the rat. Molecular Reproduction and Development 62, 547-556.