XB-ART-48552
Nat Commun
July 8, 2014;
5
3318.
Phosphorylation of ARPP19 by protein kinase A prevents meiosis resumption in Xenopus oocytes.
Abstract
During oogenesis, oocytes are arrested in prophase and resume meiosis by activating the kinase Cdk1 upon hormonal stimulation. In all vertebrates, release from prophase arrest relies on protein kinase A (PKA) downregulation and on the dephosphorylation of a long sought but still unidentified substrate. Here we show that ARPP19 is the PKA substrate whose phosphorylation at serine 109 is necessary and sufficient for maintaining Xenopus oocytes arrested in prophase. By downregulating PKA, progesterone, the meiotic inducer in Xenopus, promotes partial dephosphorylation of ARPP19 that is required for the formation of a threshold level of active Cdk1. Active Cdk1 then initiates the MPF autoamplification loop that occurs independently of both PKA and ARPP19 phosphorylation at serine 109 but requires the Greatwall (Gwl)-dependent phosphorylation of ARPP19 at serine 67. Therefore, ARPP19 stands at a crossroads in the meiotic M-phase control network by integrating differential effects of PKA and Gwl, two kinases essential for meiosis resumption.
PubMed ID: 24525567
PMC ID: PMC4014304
Article link: Nat Commun
Grant support: [+]
Species referenced: Xenopus laevis
Genes referenced: ankrd2 arpp19 ccnb1.2 ccnb2 cdc27 cdk1 lyz mapk1 mastl mos pkmyt1 plk1 ppp2r2d
Antibodies: Mos Ab2
Article Images: [+] show captions
References [+] :
Abrieu,
The Polo-like kinase Plx1 is a component of the MPF amplification loop at the G2/M-phase transition of the cell cycle in Xenopus eggs.
1999, Pubmed,
Xenbase
Abrieu,
The Polo-like kinase Plx1 is a component of the MPF amplification loop at the G2/M-phase transition of the cell cycle in Xenopus eggs.
1999,
Pubmed
,
Xenbase
Bontron, Yeast endosulfines control entry into quiescence and chronological life span by inhibiting protein phosphatase 2A. 2013, Pubmed , Xenbase
Boyer, Progesterone and cAMP-dependent protein kinase regulate in vivo the level of phosphorylation of two proteins (Mr 20,000 and Mr 32,000) in Xenopus oocytes. 1986, Pubmed , Xenbase
Bradford, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. 1976, Pubmed
Cameroni, The novel yeast PAS kinase Rim 15 orchestrates G0-associated antioxidant defense mechanisms. 2004, Pubmed
Conti, Role of cyclic nucleotide signaling in oocyte maturation. 2002, Pubmed , Xenbase
Daar, Inhibition of mos-induced oocyte maturation by protein kinase A. 1993, Pubmed , Xenbase
Duckworth, G2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A. 2002, Pubmed , Xenbase
Dulubova, ARPP-16/ARPP-19: a highly conserved family of cAMP-regulated phosphoproteins. 2001, Pubmed
Dupré, The phosphorylation of ARPP19 by Greatwall renders the auto-amplification of MPF independently of PKA in Xenopus oocytes. 2013, Pubmed , Xenbase
Dupré, Mos is not required for the initiation of meiotic maturation in Xenopus oocytes. 2002, Pubmed , Xenbase
Eyers, Regulation of the G(2)/M transition in Xenopus oocytes by the cAMP-dependent protein kinase. 2005, Pubmed , Xenbase
Fernandez, Implications for cAMP-dependent protein kinase in the maintenance of the interphase state. 1998, Pubmed
Frank-Vaillant, Two distinct mechanisms control the accumulation of cyclin B1 and Mos in Xenopus oocytes in response to progesterone. 1999, Pubmed , Xenbase
Gaffré, A critical balance between Cyclin B synthesis and Myt1 activity controls meiosis entry in Xenopus oocytes. 2011, Pubmed , Xenbase
Gharbi-Ayachi, The substrate of Greatwall kinase, Arpp19, controls mitosis by inhibiting protein phosphatase 2A. 2010, Pubmed , Xenbase
Goris, Okadaic acid, a specific protein phosphatase inhibitor, induces maturation and MPF formation in Xenopus laevis oocytes. 1989, Pubmed , Xenbase
Grieco, A role for cAMP-dependent protein kinase in early embryonic divisions. 1994, Pubmed , Xenbase
Grieco, Requirement for cAMP-PKA pathway activation by M phase-promoting factor in the transition from mitosis to interphase. 1996, Pubmed , Xenbase
Haccard, Induction of Xenopus oocyte meiotic maturation by MAP kinase. 1995, Pubmed , Xenbase
Haccard, Redundant pathways for Cdc2 activation in Xenopus oocyte: either cyclin B or Mos synthesis. 2006, Pubmed , Xenbase
Haccard, Oocyte maturation, Mos and cyclins--a matter of synthesis: two functionally redundant ways to induce meiotic maturation. 2006, Pubmed
Han, Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. 2005, Pubmed , Xenbase
Hara, Greatwall kinase and cyclin B-Cdk1 are both critical constituents of M-phase-promoting factor. 2012, Pubmed , Xenbase
Huchon, The pure inhibitor of cAMP-dependent protein kinase initiates Xenopus laevis meiotic maturation. A 4-step scheme for meiotic maturation. 1981, Pubmed , Xenbase
Inoue, The Polo-like kinase Plx1 interacts with and inhibits Myt1 after fertilization of Xenopus eggs. 2005, Pubmed , Xenbase
Juanes, Budding yeast greatwall and endosulfines control activity and spatial regulation of PP2A(Cdc55) for timely mitotic progression. 2013, Pubmed , Xenbase
Karaiskou, From progesterone to active Cdc2 in Xenopus oocytes: a puzzling signalling pathway. 2001, Pubmed , Xenbase
Karaïskou, Phosphatase 2A and polo kinase, two antagonistic regulators of cdc25 activation and MPF auto-amplification. 1999, Pubmed , Xenbase
Kim, Decreased levels of ARPP-19 and PKA in brains of Down syndrome and Alzheimer's disease. 2001, Pubmed
Kurokawa, Cyclic AMP delays G2 progression and prevents efficient accumulation of cyclin B1 proteins in mouse macrophage cells. 1999, Pubmed
Laemmli, Cleavage of structural proteins during the assembly of the head of bacteriophage T4. 1970, Pubmed
Li, Greatwall kinase is required for meiotic maturation in porcine oocytes. 2013, Pubmed
Maller, Progesterone-stimulated meiotic cell division in Xenopus oocytes. Induction by regulatory subunit and inhibition by catalytic subunit of adenosine 3':5'-monophosphate-dependent protein kinase. 1977, Pubmed , Xenbase
Maller, Early effect of progesterone on levels of cyclic adenosine 3':5'-monophosphate in Xenopus oocytes. 1979, Pubmed , Xenbase
Masciarelli, Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. 2004, Pubmed
Masui, Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. 1971, Pubmed
Matten, Protein kinase A acts at multiple points to inhibit Xenopus oocyte maturation. 1994, Pubmed , Xenbase
Mochida, Greatwall phosphorylates an inhibitor of protein phosphatase 2A that is essential for mitosis. 2010, Pubmed , Xenbase
Morgan, Principles of CDK regulation. 1995, Pubmed
Mulner, Cyclic AMP synthesis in Xenopus laevis oocytes: inhibition by progesterone. 1979, Pubmed , Xenbase
Nakajo, Absence of Wee1 ensures the meiotic cell cycle in Xenopus oocytes. 2000, Pubmed , Xenbase
Ozon, Roles of cyclic AMP and calcium in maturation of Xenopus laevis oocytes. 1979, Pubmed , Xenbase
Palmer, A link between MAP kinase and p34(cdc2)/cyclin B during oocyte maturation: p90(rsk) phosphorylates and inactivates the p34(cdc2) inhibitory kinase Myt1. 1998, Pubmed , Xenbase
Peter, A new role for Mos in Xenopus oocyte maturation: targeting Myt1 independently of MAPK. 2002, Pubmed , Xenbase
Rime, Microinjection of Cdc25 protein phosphatase into Xenopus prophase oocyte activates MPF and arrests meiosis at metaphase I. 1995, Pubmed , Xenbase
Rime, Characterization of MPF activation by okadaic acid in Xenopus oocyte. 1990, Pubmed , Xenbase
Rime, Activation of p34cdc2 kinase by cyclin is negatively regulated by cyclic amp-dependent protein kinase in Xenopus oocytes. 1992, Pubmed , Xenbase
Sagata, The product of the mos proto-oncogene as a candidate "initiator" for oocyte maturation. 1989, Pubmed , Xenbase
Schägger, Tricine-SDS-PAGE. 2007, Pubmed
Sheppard, Cyclic AMP levels in synchronized mammalian cells. 1973, Pubmed
Smith, The induction of oocyte maturation: transmembrane signaling events and regulation of the cell cycle. 1990, Pubmed
Stambrook, Reversible arrest of Chinese hamster V79 cells in G2 by dibutytyl AMP. 1976, Pubmed
Studier, Protein production by auto-induction in high density shaking cultures. 2005, Pubmed
Taylor, Assembly of allosteric macromolecular switches: lessons from PKA. 2012, Pubmed
Thomas, Expression in Escherichia coli and characterization of the heat-stable inhibitor of the cAMP-dependent protein kinase. 1991, Pubmed
Wang, Direct roles of the signaling kinase RSK2 in Cdc25C activation during Xenopus oocyte maturation. 2010, Pubmed , Xenbase
Wang, Progesterone inhibits protein kinase A (PKA) in Xenopus oocytes: demonstration of endogenous PKA activities using an expressed substrate. 2004, Pubmed , Xenbase
Wasserman, Effects of cyclohexamide on a cytoplasmic factor initiating meiotic naturation in Xenopus oocytes. 1975, Pubmed , Xenbase
Zhao, Roles of Greatwall kinase in the regulation of cdc25 phosphatase. 2008, Pubmed , Xenbase
Bontron, Yeast endosulfines control entry into quiescence and chronological life span by inhibiting protein phosphatase 2A. 2013, Pubmed , Xenbase
Boyer, Progesterone and cAMP-dependent protein kinase regulate in vivo the level of phosphorylation of two proteins (Mr 20,000 and Mr 32,000) in Xenopus oocytes. 1986, Pubmed , Xenbase
Bradford, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. 1976, Pubmed
Cameroni, The novel yeast PAS kinase Rim 15 orchestrates G0-associated antioxidant defense mechanisms. 2004, Pubmed
Conti, Role of cyclic nucleotide signaling in oocyte maturation. 2002, Pubmed , Xenbase
Daar, Inhibition of mos-induced oocyte maturation by protein kinase A. 1993, Pubmed , Xenbase
Duckworth, G2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A. 2002, Pubmed , Xenbase
Dulubova, ARPP-16/ARPP-19: a highly conserved family of cAMP-regulated phosphoproteins. 2001, Pubmed
Dupré, The phosphorylation of ARPP19 by Greatwall renders the auto-amplification of MPF independently of PKA in Xenopus oocytes. 2013, Pubmed , Xenbase
Dupré, Mos is not required for the initiation of meiotic maturation in Xenopus oocytes. 2002, Pubmed , Xenbase
Eyers, Regulation of the G(2)/M transition in Xenopus oocytes by the cAMP-dependent protein kinase. 2005, Pubmed , Xenbase
Fernandez, Implications for cAMP-dependent protein kinase in the maintenance of the interphase state. 1998, Pubmed
Frank-Vaillant, Two distinct mechanisms control the accumulation of cyclin B1 and Mos in Xenopus oocytes in response to progesterone. 1999, Pubmed , Xenbase
Gaffré, A critical balance between Cyclin B synthesis and Myt1 activity controls meiosis entry in Xenopus oocytes. 2011, Pubmed , Xenbase
Gharbi-Ayachi, The substrate of Greatwall kinase, Arpp19, controls mitosis by inhibiting protein phosphatase 2A. 2010, Pubmed , Xenbase
Goris, Okadaic acid, a specific protein phosphatase inhibitor, induces maturation and MPF formation in Xenopus laevis oocytes. 1989, Pubmed , Xenbase
Grieco, A role for cAMP-dependent protein kinase in early embryonic divisions. 1994, Pubmed , Xenbase
Grieco, Requirement for cAMP-PKA pathway activation by M phase-promoting factor in the transition from mitosis to interphase. 1996, Pubmed , Xenbase
Haccard, Induction of Xenopus oocyte meiotic maturation by MAP kinase. 1995, Pubmed , Xenbase
Haccard, Redundant pathways for Cdc2 activation in Xenopus oocyte: either cyclin B or Mos synthesis. 2006, Pubmed , Xenbase
Haccard, Oocyte maturation, Mos and cyclins--a matter of synthesis: two functionally redundant ways to induce meiotic maturation. 2006, Pubmed
Han, Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. 2005, Pubmed , Xenbase
Hara, Greatwall kinase and cyclin B-Cdk1 are both critical constituents of M-phase-promoting factor. 2012, Pubmed , Xenbase
Huchon, The pure inhibitor of cAMP-dependent protein kinase initiates Xenopus laevis meiotic maturation. A 4-step scheme for meiotic maturation. 1981, Pubmed , Xenbase
Inoue, The Polo-like kinase Plx1 interacts with and inhibits Myt1 after fertilization of Xenopus eggs. 2005, Pubmed , Xenbase
Juanes, Budding yeast greatwall and endosulfines control activity and spatial regulation of PP2A(Cdc55) for timely mitotic progression. 2013, Pubmed , Xenbase
Karaiskou, From progesterone to active Cdc2 in Xenopus oocytes: a puzzling signalling pathway. 2001, Pubmed , Xenbase
Karaïskou, Phosphatase 2A and polo kinase, two antagonistic regulators of cdc25 activation and MPF auto-amplification. 1999, Pubmed , Xenbase
Kim, Decreased levels of ARPP-19 and PKA in brains of Down syndrome and Alzheimer's disease. 2001, Pubmed
Kurokawa, Cyclic AMP delays G2 progression and prevents efficient accumulation of cyclin B1 proteins in mouse macrophage cells. 1999, Pubmed
Laemmli, Cleavage of structural proteins during the assembly of the head of bacteriophage T4. 1970, Pubmed
Li, Greatwall kinase is required for meiotic maturation in porcine oocytes. 2013, Pubmed
Maller, Progesterone-stimulated meiotic cell division in Xenopus oocytes. Induction by regulatory subunit and inhibition by catalytic subunit of adenosine 3':5'-monophosphate-dependent protein kinase. 1977, Pubmed , Xenbase
Maller, Early effect of progesterone on levels of cyclic adenosine 3':5'-monophosphate in Xenopus oocytes. 1979, Pubmed , Xenbase
Masciarelli, Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. 2004, Pubmed
Masui, Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. 1971, Pubmed
Matten, Protein kinase A acts at multiple points to inhibit Xenopus oocyte maturation. 1994, Pubmed , Xenbase
Mochida, Greatwall phosphorylates an inhibitor of protein phosphatase 2A that is essential for mitosis. 2010, Pubmed , Xenbase
Morgan, Principles of CDK regulation. 1995, Pubmed
Mulner, Cyclic AMP synthesis in Xenopus laevis oocytes: inhibition by progesterone. 1979, Pubmed , Xenbase
Nakajo, Absence of Wee1 ensures the meiotic cell cycle in Xenopus oocytes. 2000, Pubmed , Xenbase
Ozon, Roles of cyclic AMP and calcium in maturation of Xenopus laevis oocytes. 1979, Pubmed , Xenbase
Palmer, A link between MAP kinase and p34(cdc2)/cyclin B during oocyte maturation: p90(rsk) phosphorylates and inactivates the p34(cdc2) inhibitory kinase Myt1. 1998, Pubmed , Xenbase
Peter, A new role for Mos in Xenopus oocyte maturation: targeting Myt1 independently of MAPK. 2002, Pubmed , Xenbase
Rime, Microinjection of Cdc25 protein phosphatase into Xenopus prophase oocyte activates MPF and arrests meiosis at metaphase I. 1995, Pubmed , Xenbase
Rime, Characterization of MPF activation by okadaic acid in Xenopus oocyte. 1990, Pubmed , Xenbase
Rime, Activation of p34cdc2 kinase by cyclin is negatively regulated by cyclic amp-dependent protein kinase in Xenopus oocytes. 1992, Pubmed , Xenbase
Sagata, The product of the mos proto-oncogene as a candidate "initiator" for oocyte maturation. 1989, Pubmed , Xenbase
Schägger, Tricine-SDS-PAGE. 2007, Pubmed
Sheppard, Cyclic AMP levels in synchronized mammalian cells. 1973, Pubmed
Smith, The induction of oocyte maturation: transmembrane signaling events and regulation of the cell cycle. 1990, Pubmed
Stambrook, Reversible arrest of Chinese hamster V79 cells in G2 by dibutytyl AMP. 1976, Pubmed
Studier, Protein production by auto-induction in high density shaking cultures. 2005, Pubmed
Taylor, Assembly of allosteric macromolecular switches: lessons from PKA. 2012, Pubmed
Thomas, Expression in Escherichia coli and characterization of the heat-stable inhibitor of the cAMP-dependent protein kinase. 1991, Pubmed
Wang, Direct roles of the signaling kinase RSK2 in Cdc25C activation during Xenopus oocyte maturation. 2010, Pubmed , Xenbase
Wang, Progesterone inhibits protein kinase A (PKA) in Xenopus oocytes: demonstration of endogenous PKA activities using an expressed substrate. 2004, Pubmed , Xenbase
Wasserman, Effects of cyclohexamide on a cytoplasmic factor initiating meiotic naturation in Xenopus oocytes. 1975, Pubmed , Xenbase
Zhao, Roles of Greatwall kinase in the regulation of cdc25 phosphatase. 2008, Pubmed , Xenbase