4E-BP1 degradation and eIF4E truncation occur spatially distinctly in the porcine uterine epithelia and are features of noninvasive implantation in the pig

Molecular Reproduction and Development

Volumn 78, Issue 12, 2011, Pages 895-905

  Wollenhaupt, Karin ^a   Reinke, Kati ^a   Brüssow, Klaus Peter ^a   Kanitz, Wilhelm ^a   Tomek, Wolfgang ^a  

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

Author keywords

4E BP1; EIF4E; Endometrium; Implantation; Translation initiation

Indexed keywords

ESTRADIOL; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 1; INITIATION FACTOR 4G; PROGESTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOASSAY; CELL FRACTIONATION; CELL LYSATE; ENDOMETRIUM; FEMALE; IMPLANTATION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; SWINE; TRANSLATION INITIATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CALCIUM; EMBRYO IMPLANTATION; ENDOMETRIUM; EPITHELIUM; EUKARYOTIC INITIATION FACTOR-4E; FEMALE; HISTOCYTOCHEMISTRY; PEPTIDE HYDROLASES; PHOSPHOPROTEINS; PHOSPHORYLATION; PREGNANCY; REPRESSOR PROTEINS; SWINE;

SUIDAE; SUS;

EID: 81355160669     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.21376     Document Type: Article

References (47)

1. Bazer FW. 1975. Uterine protein secretions: Relationship to development of the conceptus. J Anim Sci 41: 1376-1382.
2. Bazer FW, Spencer TE, Ott TL. 1998. Endocrinology of the transition from recurring estrous cycles to establishment of pregnancy in subprimate mammals. In: Bazer FW, editor. The endocrinology of pregnancy. Totowa, NJ: Humana Press Inc. pp 1-34.
3. Bazer FW, Burghardt RC, Johnson GA, Spencer TE, Wu G. 2008. Interferons and progesterone for establishment and maintenance of pregnancy: Interactions among novel cell signaling pathways. Reprod Biol 8: 179-211.
4. Bhojwani M, Rudolph E, Kanitz W, Zuehlke H, Schneider F, Tomek W. 2006. Molecular analysis of maturation processes by protein and phosphoprotein profiling during in vitro maturation of bovine oocytes: A proteomic approach. Cloning Stem Cells 8: 259-274.
5. Blitek A, Ziecik AJ. 2004. Prostaglandins F2α and E2 secretion by porcine epithelial and stromal endometrial cells on different days of the oestrous cycle. Reprod Dom Anim 39: 340-346.
6. Borman AM, Michel YM, Kean KM. 2000. Biochemical characterisation of cap-poly(A) synergy in rabbit reticulocyte lysates: The eIF4G-PABP interaction increases the functional affinity of eIF4E for the capped mRNA 5'-end. Nucleic Acids Res 28: 4068-4075.
7. Braunstein S, Badura ML, Xi Q, Formenti SC, Schneider RJ. 2009. Regulation of protein synthesis by ionizing radiation. Mol Cell Biol 29: 5645-5656.
8. Clark JG, Schrader WT, ÓMalley BW. 1985. Mechanisms of steroid hormone action. In: Wilson JD, Foster DW, editors. Textbook of endocrinol. Philadelphia: EB Saunders. pp 33-75.
9. Dery MC, Leblanc V, Shooner C, Asselin E. 2003. Regulation of Akt expression and phosphorylation by 17β-estradiol in the rat uterus during estrous cycle. Reprod Biol Endocrinol 1: 1-13.
10. Dua K, Williams TM, Beretta L. 2001. Translational control of the proteome: Relevance to cancer. Proteomics 1: 1191-1199.
11. 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.
12. Ellederová Z, Cais O, Susor A, Uhlírová K, Kovárová H, Jelínková L, Tomek W, Kubelka M. 2008. ERK1/2 map kinase metabolic pathway is responsible for phosphorylation of translation initiation factor eIF4E during in vitro maturation of pig oocytes. Mol Reprod Dev 75: 309-317.
13. Geisert RD, Renegar RH, Thatcher WW, Roberts RM, Bazer FM. 1982. Establishment of pregnancy in pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions. Endocrinology 27: 925-939.
14. Geisert RD, Zavy MT, Moffatt RJ, Blair RM, Yellin T. 1990. Embryonic steroids and the establishment of pregnancy in pigs. J Reprod Fertil Suppl 40: 293-305.
15. Gingras AC, Raugth B, Gygi SP, Niedzwiecka A, Miron M, Burley SK, Polakiewicz RD, Wyslouch-Cieszynska A, Aebersold R, Sonenberg N. 2001. Hierarchical phosphorylation of the translational inhibitor 4E-BP1. Genes Dev 15: 2852-2864.
16. Gray CA, Bartol FF, Tarleton BJ, Wiley AA, Johnson GA, Bazer FW, Spencer TE. 2001. Developmental biology of uterine glands. Biol Reprod 65: 1311-1323.
17. 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: Cold Spring Harbor Laboratory Press. pp 33-126.
18. Johnes RM, Branda J, Johnston KA, Polymenis M, Gadd M, Rustgi A, Callanan L, Schmidt EV. 1996. An essential E box in the promotor of the gene encoding the mRNA cap-binding protein (eukaryotic initiation factor 4E) is a target for activation by c-myc. Mol Cell Biol 16: 4754-4764.
19. Keys JL, King GJ, LaForest JP. 1989. Autofluorescence of the porcine endometrium during early pregnancy. Biol Reprod 40: 220-222.
20. Kirby M, Zsarnovszky A, Belcher SM. 2004. Estrogen receptor expression in a human primitive neuroectodermal tumor cell line from the cerebral cortex: Estrogen stimulates rapid ERK1/2 activation and receptor-dependent cell migration. Biochem Biophys Res Commun 319: 753-758.
21. Krzymowski T, Stefanczyk-Krzymowska S. 2002. Uterine blood supply as a main factor involved in the regulation of the estrous cycle-A new theory. Reprod Biol 2: 93-114.
22. Lengyel F, Vertes Z, Kovacs KA, Környei JL, Sumegi B, Vertes M. 2004. Expression and activation of Akt/protein kinase B in sexually immature and mature rat uterus. J Steroid Biochem Mol Biol 91: 285-288.
23. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
24. Menino AR, Hogan A, Schultz GA, Novak S, Dixon W, Foxcroft GH. 1997. Expression of proteinases and proteinase inhibitors during embryo-uterine contact in the pig. Dev Genet 21: 68-74.
25. Migliaccio A, Di Domenico M, Castoria G, de Falco A, Bontempo P, Nola E, Auriccio F. 1996. Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J 15: 1292-1300.
26. Migliaccio A, Piccolo D, Castoria G, Di Domenico M, Bilancio A, Lombardi M, Gong W, Beato M, Auriccio F. 1998. Activation of Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J 17: 2008-2018.
27. Morley SJ. 1997. Signalling through either the p38 or ERK mitogen-activated protein (MAP) kinase pathway is obligatory for phorbol ester and T cell receptor complex (TCR-CD3) stimulated phosphorylation of initiation factor (eIF) 4E in Jurkat T cells. FEBS Lett 418: 327-332.
28. Østrup E, Bauersachs S, Blum H, Wolf E, Hyttel P. 2010. Differential endometrial gene expression in pregnant and non-pregnant sows. Biol Reprod 83: 277-285.
29. Polymenis M, Schmidt EV. 1999. Coordination of cell growth with cell division. Curr Opin Genet Dev 9: 76-80. Rev.
30. Pusateri AE, Smith KM, Smith JW II, Thomford PJ, Diekman MA. 1996. Maternal recognition of pregnancy in swine. I. Minimal requirement for exogenous estradiol-17β to induce either short or long pseudopregnancy in cycling gilts. Biol Reprod 55: 582-589.
31. Samuel CA, Perry JS. 1972. The ultrastructure of the pig trophoblast transplanted to an ectopic site in the uterine wall. J Anat 113: 139-149.
32. Schwanhäusser B, Dorothea Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Wei Chen W, Selbach M. 2011. Global quantification of mammalian gene expression control. Nature 473: 337-342.
33. Schweigert FJ, Bonitz K, Siegling C, Buchholz I. 1999. Distribution of vitamin A, retinol-binding protein, cellular retinoic acid-binding protein I, and retinoid X receptor b in the porcine uterus during early gestation. Biol Reprod 61: 906-911.
34. Siemer C, Smiljakovic T, Bhojwani M, Leiding C, Kanitz W, Kubelka M, Tomek W. 2009. Analysis of mRNA associated factors during bovine oocyte maturation and early embryonic development. Mol Reprod Dev 76: 1208-1219.
35. Simmen RC, Simmen FA, Hofig A, Farmer FJ, Bazer FW. 1990. Hormonal regulation of insulinlike growth factor gene expression in pig uterus. Endocrinology 127: 2166-2174.
36. Simmen FA, Simmen RC, Geisert RD, Martinat-Botte F, Bazer FW. 1992. Differential expression, during the estrous cycle and pre- and postimplantation conceptus development, of messenger ribonucleic acids encoding components of the pig uterine insulin-like growth factor system. Endocrinology 130: 1547-1556.
37. Sonenberg N. 2008. eIF4E, the mRNA cap-binding protein: from Basic discovery to translational research. Biochem Cell Biol 86: 178-183.
38. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell 136: 731-745.
39. Spencer TE, Johnson GA, Burghardt RC, Bazer FW. 2004. Progesterone and placental hormone actions on the uterus: Insights from domestic animals. Biol Reprod 71: 2-10.
40. Susor A, Jelínková L, Karabínová P, Torner H, Tomek W, Kovárová H, Kubelka M. 2008. Regulation of cap-dependent translation initiation in the early stage porcine parthenotes. Mol Reprod Dev 75: 1717-1725.
41. Tiemann U, Tomek W, Schneider F, Wollenhaupt K, Kanitz W, Becker F, Pöhland R, Alm H. 2001. Platelet-activating factor (PAF)-like activity, localization of PAF receptor (PAF-R) and PAF-acetylhydrolase (PAF-AH) activity in bovine endometrium at different stages of the estrous cycle and early pregnancy. Prostaglandins Other Lipid Mediat 65: 125-141.
42. Tomek W, Smiljakovic T. 2005. Activation of Akt (protein kinase B) stimulates metaphase I to metaphase II transition in bovine oocytes. Reproduction 130: 423-430.
43. Tomek W, Mela 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.
44. Wollenhaupt K, Tomek W, Brüssow KP, Tiemann U, Viergutz T, Schneider F, Nürnberg G. 2002. Effects of ovarian steroids and epidermal growth factor (EGF) on expression and bioactivation of specific regulators of transcription and translation in oviductal tissue in pigs. Reproduction 123: 87-96.
45. Wollenhaupt K, Brüssow KP, Tiemann U, Tomek W. 2007. The embryonic pregnancy signal oestradiol influences gene expression at the level of translational initiation in porcine endometrial cells. Reprod Dom Anim 42: 167-175.
46. Wollenhaupt K, Reinke K, Brüssow KP, Albrecht D, Tiemann U, Seyfert HM, Tomek W. 2010. Natural occurrence and physiological role of a truncated eIF4E in the porcine endometrium during implantation. Biochem J 432: 353-363.
47. Wollenhaupt K, Reinke K, Brüssow KP, Spitschak M, Kanitz W, Tomek W. 2011. Truncation of the mRNA cap-binding protein eIF4E is specific fort he non-invasive implantation in pigs. Reprod Dom Anim 46: 917-919.