ERK1/2 map kinase metabolic pathway is responsible for phosphorylation of translation initiation factor eIF4E during in vitro maturation of pig oocytes

Molecular Reproduction and Development

Volumn 75, Issue 2, 2008, Pages 309-317

  Ellederová, Zdenka ^a   Cais, Ondřej ^b   Šušor, Andrej ^a   Uhlířová, Katka ^a   Kovářová, Hana ^a   Jelínková, Lucie ^a   Tomek, Wolfgang ^c   Kubelka, Michal ^a  

^a INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

Author keywords

eIF4E phosphorylation; MAP kinase; Meiosis; Translation initiation

Indexed keywords

INITIATION FACTOR 4E; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; GILT (SWINE); IN VITRO STUDY; NONHUMAN; OOCYTE MATURATION; PRIORITY JOURNAL; SOMATIC CELL;

ANIMALS; ENZYME INHIBITORS; EUKARYOTIC INITIATION FACTOR-4E; FEMALE; ISOELECTRIC FOCUSING; MITOGEN-ACTIVATED PROTEIN KINASE 3; OOCYTES; PHOSPHORYLATION; SWINE;

EUKARYOTA; SUIDAE;

EID: 37849025187     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.20690     Document Type: Article

References (53)

1. Brevini TA, Lonergan P, Cillo F, Francisci C, Favetta LA, Fair T, Gandolfi F. 2002. Evolution of mRNA polyadenylation between oocyte maturation and first embryonic cleavage in cattle and its relation with developmental competence. Mol Reprod Dev 63:510-517.
2. Brevini-Gandolfi TA, Favetta LA, Mauri L, Luciano AM, Cillo F, Gandolfi F. 1999. Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence. Mol Reprod Dev 52:427-433.
3. Ellederova Z, Kovarova H, Melo-Sterza F, Livingstone M, Tomek W, Kubelka M. 2006. Suppression of translation during in vitro maturation of pig oocytes despite enhanced formation of cap-binding protein complex eIF4F and 4E-BP1 hyperphosphorylation. Mol Reprod Dev 73:68-76.
4. Fraser CS, Pain VM, Morley SJ. 1999b. Cellular stress in Xenopus kidney cells enhances the phosphorylation of eukaryotic translation initiation factor (eIF)4E and the association of eIF4F with poly(A)-binding protein. Biochem J 342:519-526.
5. Fukunaga R, Hunter T. 1997. MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J 16:1921-1933.
6. Gavin AC, Schorderet-Slatkine S. 1997. Ribosomal S6 kinase p90rsk and mRNA cap-binding protein eIF4E phosphorylations correlate with MAP kinase activation during meiotic reinitiation of mouse oocytes. Mol Reprod Dev 46:383-391.
7. Gebauer F, Xu W, Cooper GM, Richter JD. 1994. Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J 13:5712-5720.
8. Gingras AC, Raught B, Sonenberg N. 1999. eIF4 initiation factors: Effectors of mRNA recruitment to ribosomes and regulators of translation. Ann Rev Biochem 68:13-63.
9. Haghighat A, Sonenberg N. 1997. eIF4G dramatically enhances the binding of eIF4E to the mRNA 5′-cap structure. J Biol Chem 272:21677-21680.
10. Hershey JW. 1991. Translational control in mammalian cells. Annu Rev Biochem 60:717-755.
11. Hershey JWB, Merrick WC. 2000. Pathway and mechanism of initiation of protein synthesis. In: Sonenberg N, Hershey JWB, Mathews B, editors. Translational control of gene expression. Cold Spring Harbor: ColdSpring Harbor Laboratory Press. pp 33-126.
12. Joshi B, Cai AL, Keiper BD, Minich WB, Mendez R, Beach CM, Stepinski J, Stolarski R, Darzynkiewicz E, Rhoads RE. 1995. Phosphorylation of eukaryotic protein synthesis initiation factor 4E at Ser-209. J Biol Chem 270:14597-14603.
13. Joshi-Barve S, Rychlik W, Rhoads RE. 1990. Alteration of the major phosphorylation site of eukaryotic protein synthesis initiation factor 4E prevents its association with the 48 S initiation complex. J Biol Chem 265:2979-2983.
14. Kalous J, Kubelka M, Rimkevičová Z, Guerrier P, Motlík 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.
15. Kitagawa M, Okabe T, Ogino H, Matsumoto H, Sazuki-Takahashi I, Kokubo T, Higashi H, Saitoh S, Taya Y, Yasuda H, Ohba Y, Nishimura S, Tanaka N, Okuyama A. 1993. Butyrolactone I, a selective inhibitor of cdk2 and cdc2 kinase. Oncogene 8:2425-2432.
16. Kitagawa M, Higashi H, Sazuki-Takahashi I, Okabe T, Ogino H, Taya Y, Nishimura S, Okuyama A. 1994. A cyclin-dependent kinase inhibitor butyrolactone I, inhibits phosphorylation of Rb protein and cell cycle progression. Oncogene 9:2549-2557.
17. Kleijn M, Scheper GC, Voorma HO, Thomas AA. 1998. Regulation of translation initiation factors by signal transduction. Eur J Biochem 253:531-544.
18. Kubelka M, Anger M, Pavlok A, Kalous J, Schultz RM, Motlik J. 2002a. Activation of pig and cattle oocytes by butyrolactone I: Morphological and biochemical study. Zygote 10:47-57.
19. Kubelka M, Anger M, Kalous J, Schultz RM, Motlík J. 2002b. Chromosome condensation in pig oocytes: Lack of a requirement for either CDK1 kinase or MAP kinase activity. Mol Reprod Dev 63:110-118.
20. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
21. Lamphear BJ, Panniers R. 1990. Cap binding protein complex that restores protein synthesis in heat-shocked Ehrlich cell lysates contains highly phosphorylated eIF-4E. J Biol Chem 265:5333-5336.
22. Mader S, Lee H, Pause A, Sonenberg N. 1995. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins. Mol Cell Biol 15:4990-4997.
23. Makkinje A, Xiong H, Li M, Damuni Z. 1995. Phosphorylation of eukaryotic protein synthesis initiation factor 4E by insulin-stimulated protamine kinase. J Biol Chem 270:14824-14828.
24. Maurides PA, Akkaraju GR, Jagus R. 1989. Evaluation of protein phosphorylation state by combination of vertical slab isoelectric focusing and immunoblotting. Anal Biochem 183:144-151.
25. Mendez R, Kollmorgen G, White MF, Rhoads RE. 1997. Requirement of protein kinase C zeta for stimulation of protein synthesis by insulin. Mol Cell Biol 17:5184-5192.
26. Minich WB, Balasta ML, Goss DJ, Rhoads RE. 1994. Chromatographic resolution of in vivo phosphorylated and nonphosphorylated eukaryotic translation initiation factor eIF-4E: Increased cap affinity of the phosphorylated form. Proc Natl Acad Sci USA 91:7668-7672.
27. Morino S, Imataka H, Svitkin YV, Pestova TV, Sonenberg N. 2000. Eukaryotic translation initiation factor 4E (eIF4E) binding site and the middle one-third of eIF4GI constitute the core domain for cap-dependent translation, and the C-terminal one-third functions as a modulatory region. Mol Cell Biol 20:468-477.
28. Morley SJ. 1994. Signal transduction mechanisms in the regulation of protein synthesis. Mol Biol Rep 19:221-231.
29. Morley SJ. 1997. Intracellular signalling pathways regulating initiation factor eIF4E phosphorylation during the activation of cell growth. Biochem Soc Trans 25:503-509.
30. Morley SJ, Naegele S. 2002. Phosphorylation of eukaryotic initiation factor (eIF) 4E is not required for de novo protein synthesis following recovery from hypertonic stress in human kidney cells. J Biol Chem 277:32855-32859.
31. Morley SJ, Pain VM. 1995. Hormone-induced meiotic maturation in Xenopus oocytes occurs independently of p70s6k activation and is associated with enhanced initiation factor (eIF)-4F phosphorylation and complex formation. J Cell Sci 108:1751-1760.
32. Morley SJ, Thomas G. 1991. Intracellular messengers and the control of protein synthesis. Pharmacol Ther 50:291-319.
33. Motlík J, Šutovský P, Kalous J, Kubelka M, Moos J, Schultz RM. 1996. Co-culture with pig membrana granulose cells modulates the activity of CDK1 and MAP kinase in maturing cattle oocytes. Zygote 4:247-256.
34. Ohlmann T, Pain VM, Wood W, Rau M, Morley SJ. 1997. The proteolytic cleavage of eukaryotic initiation factor (eIF) 4G is prevented by eIF4E binding protein (PHAS-I; 4E-BP1) in the reticulocyte lysate. EMBO J 16:844-855.
35. O'Loghlen A, Gonzalez VM, Salinas M, Martin ME. 2004. Suppression of human Mnk1 by small interfering RNA increases the eukaryotic initiation factor 4F activity in HEK293T cells. FEBS Lett 578:31-35.
36. Pain VM. 1996. Initiation of protein synthesis in eukaryotic cells. Eur J Biochem 236:747-771.
37. Paynton BV, Bachvarova R. 1994. Polyadenylation and deadenylation of maternal mRNAs during oocyte growth and maturation in the mouse. Mol Reprod Dev 37:172-180.
38. Proud CG, Denton RM. 1997. Molecular mechanisms for the control of translation by insulin. Biochem J 328:329-341.
39. Pyronnet S. 2000: Phosphorylation of the cap-bindingprotein eIF4E by the MAPK-activated protein kinase Mnk1. Biochem Pharmacol 60:1237-1243.
40. Pyronnet S, Imataka H, Gingras AC, Fukunaga R, Hunter T, Sonenberg N. 1999. Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E. EMBO J 18:270-279.
41. Rychlik W, Russ MA, Rhoads RE. 1987. Phosphorylation site of eukaryotic initiation factor 4E. J Biol Chem 262:10434-10437.
42. Saghir AN, Tuxworth WJ, Jr., Hagedorn CH, McDermott PJ. 2001. Modifications of eukaryotic initiation factor 4F (eIF4F) in adult cardiocytes by adenoviral gene transfer: Differential effects on eIF4F activity and total protein synthesis rates. Biochem J 356: 557-566.
43. Scheper GC, Proud CG. 2002. Does phosphorylation of the cap-binding protein eIF4E play a role in translation initiation? Eur J Biochem 269:5350-5359.
44. Scheper GC, Thomas AA, van Wijk R. 1998. Inactivation of eukaryotic initiation factor 2B in vitro by heat shock. Biochem J 334:463-467.
45. Scheper GC, Morrice NA, Kleijn M, Proud CG. 2001: The mitogen-activated protein kinase signal-integrating kinase Mnk2 is a eukaryotic initiation factor 4E kinase with high levels of basal activity in mammalian cells. Mol Cell Biol 21:743-754.
46. Scheper GC, van Kollenburg B, Hu J, Luo Y, Goss DJ, Proud CG. 2002. Phosphorylation of eukaryotic initiation factor 4E markedly reduces its affinity for capped mRNA. J Biol Chem 277:3303-3309.
47. Scheper GC, Parra JL, Wilson M, Van Kollenburg B, Vertegaal AC, Han ZG, Proud CG. 2003. The N and C termini of the splice variants of the human mitogen-activated protein kinase-interacting kinase Mnk2 determine activity and localization. Mol Cell Biol 23:5692-5705.
48. Slentz-Kesler K, Moore JT, Lombard M, Zhang J, Hollingsworth R, Weiner MP. 2000. Identification of the human Mnk2 gene (MKNK2) through protein interaction with estrogen receptor beta. Genomics 69:63-71.
49. Sonenberg N, Gingras AC. 1998. The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Curr Opin Cell Biol 10:268-275.
50. Tomek W, Melo Sterza FA, Kubelka M, Wollenhaupt K, Torner H, Anger M, Kanitz W. 2002. Regulation of translation during in vitro maturation of bovine oocytes: The role of MAP kinase, eIF4E (cap binding protein) phosphorylation, and eIF4E-BP1. Biol Reprod 66:1274-1282.
51. Wang X, Flynn A, Waskiewicz AJ, Webb BL, Vries RG, Baines IA, Cooper JA, Proud CG. 1998. The phosphorylation of eukaryotic initiation factor eIF4E in response to phorbol esters, cell stresses, and cytokines is mediated by distinct MAP kinase pathways. J Biol Chem 273:9373-9377.
52. Waskiewicz AJ, Flynn A, Proud CG, Cooper JA. 1997. Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J 16:1909-1920.
53. Waskiewicz AJ, Johnson JC, Penn B, Mahalingam M, Kimball SR, Cooper JA. 1999. Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol Cell Biol 19:1871-1880. Mol Reprod Dev 46:383-391.