Suppression of chemically induced and spontaneous mouse oocyte activation by amp-activated protein kinase

Biology of Reproduction

Volumn 88, Issue 3, 2013, Pages

  Ya, Ru ^a   Downs, Stephen M ^a  

^a Marquette University   (United States)

Author keywords

AMP activated protein kinase; Chemically induced activation; LT SvEiJ strain; Mouse; Oocyte; Spontaneous activation

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN MAD2; STRONTIUM;

ANAPHASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL CYCLE; CHROMOSOME LOSS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME LOCALIZATION; FEMALE; M PHASE CELL CYCLE CHECKPOINT; MEIOSIS; METAPHASE; MOUSE; NONHUMAN; OOCYTE MATURATION; PRIORITY JOURNAL; PROMETAPHASE;

AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CALCIMYCIN; CELL CYCLE PROTEINS; ENZYME ACTIVATION; ETHANOL; FEMALE; MICE; MICE, INBRED C57BL; OOCYTES; RIBONUCLEOTIDES;

EID: 84877052621     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.106120     Document Type: Article

References (84)

1. Jones KT. Turning it on and off: M-phase promoting factor during meiotic maturation and fertilization. Mol Hum Reprod 2004; 10:1-5.
2. Horner VL, Wolfner MF. Transitioning from egg to embryo: triggers and mechanisms of egg activation. Dev Dyn 2008; 237:527-544.
3. 2++ signaling during mammalian fertilization: requirements, players, and adaptations. Cold Spring Harb Perspect Biol 2011; 3(4):1-23.
4. Stricker SA. Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 1999; 211:157-176.
5. Malcuit C, Kuokawa M, Fissore RA. Calcium oscillations and mammalian egg activation. J Cell Physiol 2006; 206:565-573.
6. 2++, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev Biol 2008; 315:257-279.
7. Madgwick S, Jones KT. How eggs arrest at metaphase II: MPF stabilisation plus APC/C inhibition equals Cytostatic Factor. Cell Division 2007; 2:4-11.
8. College WH, Carlton MBL, Udy GB, Evans MJ. Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature 1994; 370:65-68.
9. Hashimoto N, Watanabe N, Furuta Y, Tamemoto H, Sagata N, Yokoyama M, Okazaki K, Nagayoshi M, Takedat N, Ikawatll Y, Aizawai S. Parthenogenetic activation of oocytes in c-deficient mice. Nature 1994; 370:68-71.
10. Phillips KP, Petrunewich MAF, Collins JL, Booth RA, Liu XJ, Baltz JM. Inhibition of MEK or cdc2 kinase parthenogenetically activates mouse eggs and yields the same phenotypes as Mos-/- parthenogenotes. Dev Biol 2002; 247:210-223.
11. Shoji S, Yoshida N, Amanai M, Ohgishi M, Fukui T, Fujimoto S, Nakano Y, Kajikawa E, Perry ACF. Mammalian Emi2 mediates cytostatic arrest and transduces the signal for meiotic exit via Cdc20. EMBO J 2006; 25:834-845.
12. Madgwick S, Hansen DV, Levasseur M, Jackson PK, Jones KT. Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. J Cell Biol 2006; 174:791-801.
13. Nixon VL, Levasseur M, McDougall A, Jones KT. Ca(2+) oscillations promote APC/C-dependent cyclin B1 degradation during metaphase arrest and completion of meiosis in fertilizing mouse eggs. Curr Biol 2006; 12:746-750.
14. Suzuki T, Suzuki E, Yoshida N, Kubo A, Li H, Okuda E, Amanai M, Perry CF. Mouse Emi2 as a distinctive regulatory hub in second meiotic metaphase. Development 2010; 137:3281-3291.
15. Kaufman MH. Early Mammalian Development: Parthenogenetic Studies. London: Cambridge University Press; 1983.
16. Marston J, Chang M. The fertilizable life of ova and their morphology following delayed insemination in mature and immature mice. J Exp Zool 1964; 155:237-251.
17. Kubiak JZ. Mouse oocytes gradually develop the capacity for activation during the metaphase II arrest. Dev Biol 1989; 136:537-545.
18. Xu Z, Abbott A, Kopf GS, Schultz RM, Ducibella T. Spontaneous activation of ovulated mouse eggs: time-dependent effects on M-phase exit, cortical granule exocytosis, maternal messenger ribonucleic acid recruitment, and inositol 1,4,5-trisphosphate sensitivity. Biol Reprod 1997; 57:743-750.
19. Steinhardt RA, Epel D, Darroll EJ, Yanagimachi R. Is calcium ionophore a universal activator for unfertilized eggs? Nature 1974; 252:41-43.
20. Uranga JA, Pedersen RA, Arechaga J. Parthenogenetic activation of mouse oocytes using calcium ionophores and protein kinase C stimulators. Int J Dev Biol 1996; 40:515-519.
21. 2++. 1985; Nature 316:541-542.
22. Sun Q-Y, Rubinstein S, Breitbart H. MAP kinase activity is downregulated by phorbol ester during mouse oocyte maturation and egg activation in vitro. Mol Reprod Dev 1999; 52:310-318.
23. Siracusa G, Whittingham DG, Molinaro M, Vivarelli E. Parthenogenetic activation of mouse oocytes induced by inhibitors of protein synthesis. J Embryol Exp Morphol 1978; 43:157-166.
24. Fulka J Jr, Moor R, Fulka J. Sister chromatid separation and the metaphase-anaphase transition in mouse oocytes. Dev Biol 1994; 165:410-417.
25. Kaufman MH. The chromosome complement of single-pronuclear haploid mouse embryos following activation by ethanol treatment. J Embryol Exp Morph 1982; 71:139-154.
26. Dyban AP, Khozhai LI. Parthenogenetic development of ovulated mouse ova under the influence of ethyl alcohol. Bull Exp Biol Med 1980; 89:528-530.
27. Cuthbertson KSR. Parthenogenetic activation of mouse oocytes in vitro with ethanol and benzyl alcohol. J Exp Zool 1983; 226:311-314.
28. O'Neill GT, Rolfe LR, Kaufman MH. Developmental potential and chromosome constitution of strontium-induced mouse parthenogenones. Mol Reprod Dev 1991; 30:214-219.
29. Ma S-F, Liu X-Y, Miao D-Q, Han Z-B, Zhang X, Miao Y-L, Yanagimachi R, Tan J-H. Parthenogenetic activation of mouse oocytes by strontium chloride: a search for the best conditions. Theriogenology 2005; 64:1142-1157.
30. Cheng Y, Zhong Z, Latham KE. Strain-specific spontaneous activation during mouse oocyte maturation. Fertil Steril 2012; 98:200-206.
31. Downs SM. Stimulation of parthenogenesis in mouse ovarian follicles by inhibitors of inosine monophosphate dehydrogenase. Biol Reprod 1990; 43:427-436.
32. Downs SM, Ya R, Davis CC. Role of PRKA throughout meiotic maturation in the mouse oocyte: evidence for promotion of polar body formation and suppression of premature activation. Mol Reprod Dev 2010; 77:888-899.
33. Kaufman MH, Howlett SK. The ovulation and activation of primary and secondary oocytes in LT/Sv strain mice. Gamete Res 1986; 14:255-264.
34. Eppig JJ, Wigglesworth K. Atypical maturation of oocytes of strain I/LnJ mice. Hum Reprod 1994; 9:1136-1142.
35. Maleszewski M, Yanagimachi R. Spontaneous and sperm-induced activation of oocytes in LT/Sv strain mice. Dev Growth Differ 1995; 37:679-685.
36. Ciemerych MA, Kubiak JZ. Cytostatic activity develops during meiosis I in oocytes of LT/Sv mice. Dev Biol 1998; 200:198-211.
37. Hampl A, Eppig JJ. Analysis of the mechanism(s) of metaphase I arrest in maturing mouse oocytes. Development 1995; 121:925-933.
38. Hirao Y, Eppig JJ. Analysis of the mechanism(s) of metaphase I arrest in strain LT mouse oocytes: participation of MOS. Development 1997; 124:5107-5113.
39. Hirao Y, Eppig JJ. Analysis of the mechanism(s) of metaphase I-arrest in strain LT mouse oocytes: delay in the acquisition of competence to undergo the metaphase I/anaphase transition. Mol Reprod Dev 1999; 54:311-318.
40. Stevens LC, Varnum DS. The development of teratomas from parthenogenetically activated ovarian mouse eggs. Dev Biol 1974; 37:369-380.
41. Eppig JJ, Kozak LP, Eicher EM, Stevens LC. Ovarian teratomas in mice are derived from oocytes that have completed the first meiotic division. Nature 1977; 269:517-518.
42. Artzt K, Calo C, Pinheiro EN, Dimeo-Talento A, Tyson FL. Ovarian teratocarcinomas in LT/Sv mice carrying t-mutations. Dev Genet 1987; 8:1-9.
43. Eppig JJ, Wigglesworth K, Varnum DS, Nadeau JH. Genetic regulation of traits essential for spontaneous ovarian teratocarcinogenesis in strain LT/Sv mice: aberrant meiotic cell cycle, oocyte activation, and parthenogenetic development. Cancer Res 1996; 56:5047-5054.
44. Everett CA, Auchincloss CA, Kaufman MH, Abbott CM, West JD. Genetic influences on ovulation of primary oocytes in LT/Sv strain mice. Reproduction 2004; 128:565-571.
45. Hardie DG. PRKA: a key regulator of energy balance in the single cell and the whole organism. Int J Obesity 2008; 32:S7-S12.
46. Downs SM, Hudson ER, Hardie DG. A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes. Dev Biol 2002; 245:200-212.
47. Downs SM, Chen J. Induction of meiotic maturation in mouse oocytes by adenosine analogs. Mol Reprod Dev 2006; 73:1159-1168.
48. Chen J, Downs SM. AMP-activated protein kinase is involved in hormone-induced mouse oocyte meiotic maturation in vitro. Dev Biol 2008; 313:47-57.
49. Ya R, Downs SM. Perturbing microtubule integrity blocks AMP-activated protein kinase-induced meiotic resumption in cultured mouse oocytes. Zygote 2013; (in press). Published online ahead of print 16 November 2012; DOI http://dx.doi.org/10.1017/S0967199412000457.
50. Whittingham D, Siracusa G. The involvement of calcium in the activation of mammalian oocytes. Exp Cell Res 1978; 113:311-317.
51. Vingtdeux V, Chandakka P, Zhao H, Davies P, Marambaud P. Smallmolecule activators of AMP-activated protein kinase (PRKA), RSVA314 and RSVA405, inhibit adipogenesis. Mol Med 2011; 17:1022-1030.
52. O'Neill GT, Kaufman PMH. Ovulation and fertilization of primary and secondary oocytes in LT/Sv strain mice. Gamete Res 1987; 18:27-36.
53. Hupalowska A, Kalaszczynska I, Hoffmann S, Tsurumi C, Kubiak JZ, Polanski Z, Ciemerych MA. Metaphase I arrest in LT/Sv mouse oocytes involves the spindle assembly checkpoint. Biol Reprod 2008; 79:1102-1110.
54. Waters JC, Chen RH, Murray AW, Salmon ED. Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J Cell Biol 1998; 141:1181-1191.
55. Bos-Mikich A, Swann K, Whittingham DG. Calcium oscillations and protein synthesis inhibition synergistically activate mouse oocytes. Mol Reprod Dev 1995; 41:84-90.
56. Alberio R, Zakhartchenko V, Motlik J, Wolf E. Mammalian oocyte activation: lessons from the sperm and implications for nuclear transfer. Int J Dev Biol 2001; 45:797-809.
57. Eppig JJ. The relationship between parthenogenetic embryonic development and cumulus cell-oocyte intercellular coupling during oocyte meiotic maturation. Gamete Res 1982; 5:229-237.
58. Eppig JJ, Wigglesworth K, Hirao Y. Metaphase I arrest and spontaneous parthenogenetic activation of strain LTXBO oocytes: chimeric reaggregated ovaries establish primary lesion in oocytes. Dev Biol 2000; 224:60-68.
59. MacNicol AM, Muslin AJ, Howard EL, Kikuchi A, MacNicol MC, Williams LT. Regulation of Raf-1-dependent signaling during early Xenopus development. Mol Cell Biol 1995; 15:6686-6693.
60. Daar I, Paules RS, Vande Woude GF. A characterization of cytostatic factor activity from Xenopus eggs and c-most-transformed cells. J Cell Biol 1991; 114:329-335.
61. Tong C, Fan HY, Chen DY, Song XF, Schatten H, Sun QY. Effects of MEK inhibitor U0126 on meiotic progression in mouse oocytes: microtubule organization, asymmetric division and metaphase II arrest. Cell Res 2003; 13:375-383.
62. Zhang D, Pan L, Yang L-H, He X-K, Huang X-Y, Sun F-Z. Strontium promotes calcium oscillations in mouse meiotic oocytes and early embryos through InsP3 receptors, and requires activation of phospholipase and the synergistic action of InsP3. Hum Reprod 2005; 20:3053-3061.
63. Ross PJ, Beyhan Z, Iager AE, Yoon S-Y, Malcuit C, Schellander K, Fissore RA, Cibelli JB. Parthenogenetic activation of bovine oocytes using bovine and murine phospholipase C zeta. BMC Dev Biol 2008; 8:1-12.
64. Nakagawa K, Yamano S, Nakasaka H, Hinokio K, Yoshizawa M, Aono T. A combination of calcium ionophore and puromycin effectively produces human parthenogenones with one haploid pronucleus. Zygote 2001; 9:83-88.
65. Nakasaka H, Yamano S, Hinokio K, Nakagawa K, Yoshizawa M, Aono T. Effective activation method with A23187 and puromycin to produce haploid parthenogenones from freshly ovulated mouse oocytes. Zygote 2000; 8:203-208.
66. Lu Q, Zhao Y, Gao X, Li Y, Ma S, Mullen S, Critser JK, Chen Z-J. Combination of calcium ionophore A23187 with puromycin salvages human unfertilized oocytes after ICSI. Eur J Obstet Gynecol Reprod Biol 2006; 126:72-76.
67. 2++ increases in exponential phases during mouse oocyte activation. Nature 1981; 294:754-757.
68. Winston NJ, McGuinness O, Johnson MH, Maro B. The exit of mouse oocytes from meiotic M-phase requires an intact spindle during intracellular calcium release. J Cell Sci 1995; 108:143-151.
69. Chen R-H, Waters JC, Salmon ED, Murray AW. Association of spindle assembly checkpoint component XMad2 with unattached kinetochores. Science 1996; 274:242-246.
70. Li Y, Benezra R. Identification of a human mitotic checkpoint gene: hsMad2. Science 1994; 274:246-248.
71. Waters JC, Chen R-H, Murray AW, Gorbsky GJ, Salmon ED, Nicklas RB. Mad2 binding by phosphorylated kinetochores links error detection and checkpoint action in mitosis. Curr Biol 1996; 9:649-652.
72. Zhang D, Ma W, Li YH, Hou Y, Li SW, Meng XQ, Sun XF, Sun QY, Wang WH. Intra-oocyte localization of MAD2 and its relationship with kinetochores, microtubules, and chromosomes in rat oocytes during meiotic. Biol Reprod 2004; 71:740-748.
73. Wassmann K, Niault T, Maro B. Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr Biol 2003; 13:1596-1608.
74. Homer HA, McDougall A, Levasseur M, Murdoch AP, Herbert M. Mad2 is required for inhibiting securin and cyclin B degradation following spindle depolymerisation in meiosis I mouse oocytes. Reproduction 2005; 130:829-843.
75. Wang J-W, Lei Z-L, Nan C-L, Yin S, Liu J, Hou Y, Li Y-L, Chen D-Y, Sun Q-Y. RNA interference as a tool to study the function of MAD2 in mouse oocyte meiotic maturation. Mol Reprod Dev 2007; 74:116-124.
76. Maciejewska Z, Polanski Z, Kisiel K, Kubiak JZ, Ciemerych M. Spindle assembly checkpoint-related failure perturbs early embryonic divisions and reduces reproductive performance of LT/Sv mice. Reproduction 2009; 137:931-942.
77. Hoffmann S, Krol M, Polanski Z. Spindle assembly checkpoint-related meiotic defect in oocytes from LT/Sv mice has cytoplasmic origin and diminishes in older females. Reproduction 2012; 144:331-338.
78. Dumont J, Million K, Sunderland K, Rassinier P, Lim H, Leader B, Verlhac M-H. Formin-2 is required for spindle migration and for the late steps of cytokinesis in mouse oocytes. Dev Biol 2007; 301:254-265.
79. Pfender S, Kuznetsov V, Pleiser S, Kerkoff E, Shuh M. Spire-type actin nucleators cooperate with formin-2 to drive asymmetric oocyte division. Curr Biol 2011; 21:955-960.
80. Lee JH, Koh H, Kim M, Kim Y, Lee SY, Karess RE, Lee S-H, Shong M, Kim J-M, Kim J, Chung J. Energy-dependent regulation of cell structure by AMP-activated protein kinase. Nature 2007; 447:1017-1020.
81. Thaiparambil JT, Eggers CM, Marcus AI. PRKA regulates mitotic spindle orientation through phosphorylation of myosin regulatory light chain. Mol Cell Biol 2012; 32:3203-3217.
82. Vasquez-Martin A, Cufi S, Oliveras-Ferraros O, Menendez JA. Polo-like kinase 1 regulates activation of AMP-activated protein kinase (PRKA) at the mitotic apparatus. Cell Cycle 2012; 11:2422-2426.
83. Albertini D, Eppig JJ. Unusual cytoskeletal and chromatin configurations in mouse oocytes that are atypical in meiotic progression. Dev Genet 1995; 16:13-19.
84. Viollet B, Athea Y, Mounier R, Guigas B, Zarrinpashneh E, Horman S, Lantier L, Hebrard S, Devin-Leclerc J, Beauloye C, Foretz M, Andreelli F, et al. PRKA: lessons from transgenic and knockout animals. Front Biosci 2009; 14:19-44.