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In X. laevis embryos high levels of the anti-apoptotic factor p27BBP/eIF6 are stage-dependently found in BrdU and TUNEL-reactive territories

Published online by Cambridge University Press:  27 July 2010

N. De Marco*
Affiliation:
Department of Structural and Functional Biology, University of Naples Federico II, Naples, Italy.
C. Campanella
Affiliation:
Department of Structural and Functional Biology, University of Naples Federico II, Naples, Italy.
R. Carotenuto
Affiliation:
Department of Structural and Functional Biology, University of Naples Federico II, Naples, Italy.
*
All correspondence to: N. De Marco. Department of Structural and Functional Biology, University of Naples Federico II, Naples, Italy. Tel: +39 081 679189. Fax: +39 081 679233. e-mail: nademarc@unina.it

Summary

p27BBP/eIF6 (β4 binding protein/eukaryotic initiation factor 6) is a highly conserved protein necessary for cell life. In adult eIF6 mice, a 50% decrease in the protein levels in all tissues is accompanied by a reduction in cell proliferation only in the liver, fat cells and cultured fibroblasts. During X. laevis embryogenesis expression of p27BBP/eIF6 is abundant in high proliferative territories. However, in Xenopus cell proliferation appears unaffected following p27BBP/eIF6 over-expression or down-regulation. Indeed, p27BBP/eIF6 is an anti-apoptotic factor acting upstream of Bcl2 that reduces endogenous apoptosis. We studied p27BBP/eIF6 protein localization in wild type embryos and compared it to proliferation and apoptosis. At the beginning of embryogenesis, high levels of p27BBP/eIF6, proliferation and apoptosis overlap. In later development stages high proliferation levels are present in the same regions where higher p27BBP/eIF6 expression is observed, while apoptosis does not appear specifically concentrated in the same sites. The higher presence of p27BBP/eIF6 would appear related to an increased need of apoptosis control in the regions where cell death is essential for normal development.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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References

Biffo, S., Sanvito, F., Costa, S., Preve, L., Pignatelli, R., Spinardi, L. & Marchisio, P.C. (1997). Isolation of a novel β4 integrin binding protein (p27BBP) highly expressed in epithelial cells. J. Biol. Chem. 272, 30314–21.CrossRefGoogle ScholarPubMed
Carotenuto, R., De Marco, N., Biffo, S., Wilding, M., Vaccaro, M.C., Marchisio, P.C., Capriglione, T., Russo, G.L. & Campanella, C. (2005). Phosphorylation of p27BBP/elF6 and its association with the cytoskeleton are developmentally regulated in Xenopus oogenesis. Cell. Mol. Life Sci. 62, 1641–52.CrossRefGoogle Scholar
Ceci, M., Gaviraghi, C., Gorrini, C., Sala, L.A., Offenhauser, N., Marchisio, P.C. & Biffo, S. (2003). Release of elF6 (p27BBP) from the 6OS subunit allows 80S ribosome assembly. Nature 426, 579–84.CrossRefGoogle Scholar
De Marco, N., Iannone, L., Carotenuto, R., Biffo, S., Vitale, A. & Campanella, C. (2010). p27(BBP)/eIF6 acts as an anti-apoptotic factor upstream of Bcl-2 during Xenopus laevis development. Cell Death Differ. 17, 360–72.CrossRefGoogle ScholarPubMed
Donadini, A., Giodini, A., Sanvito, F., Marchisio, P.C. & Biffo, S. (2001). The human ITGB4BP gene is constitutively expressed in vitro, but highly modulated in vivo. Gene 266, 3543.Google ScholarPubMed
Eagleson, G., Ferreiro, B. & Harris, W.A. (1995). Fate of the anterior neural ridge and the morphogenesis of the Xenopus forebrain. J. Neurobiol. 28, 146–58.CrossRefGoogle ScholarPubMed
Finkielstein, C.V., Lewellyn, A.L. & Maller, J.L. (2001). The midblastula transition in Xenopus embryos activates multiple pathways to prevent apoptosis in response to DNA damage. Proc. Natl. Acad. Sci. USA 98, 1006–11.CrossRefGoogle ScholarPubMed
Gandin, V., Miluzio, A., Barbieri, A., Magri, L., Kiyokawa, H., Marchisio, P.C. & Biffo, S. (2008). eIF6 is rate limiting for translation, growth and transformation. Nature 455: 684–8.CrossRefGoogle ScholarPubMed
Harland, R.M. (1991). In situ hybridization: an improved whole mount method for Xenopus embryos. Meth. Cell. Biol. 36, 675685.Google ScholarPubMed
Hensey, C. & Gautier, J. (1997). A developmental timer that regulates apoptosis at the onset of gastrulation. Mech. Dev. 69, 183–95.CrossRefGoogle ScholarPubMed
Hensey, C. & Gautier, J. (1998). Programmed cell death during Xenopus development: a spatio-temporal analysis. Dev. Biol. 203, 3648.CrossRefGoogle ScholarPubMed
Holt, C.E., Bertsch, T.W., Ellis, H.M. & Harris, W.A. (1988). Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1, 1526.CrossRefGoogle ScholarPubMed
Ji, Y., Shah, S., Soanes, K., Islam, M.N., Hoxter, B., Biffo, S., Heslip, T. & Byers, S. (2008). Eukaryotic initiation factor 6 selectively regulates Wnt signalling and β-catenin protein synthesis. Oncogene 27, 755–62.CrossRefGoogle ScholarPubMed
Johns, P.R. (1977). Growth of the adult goldfish eye. III. Source of the new retinal cells. J. Comp. Neurol. 176, 343–57.CrossRefGoogle ScholarPubMed
Miluzio, A., Beugnet, A., Volta, V. & Biffo, S. (2009). Eukaryotic initiation factor 6 mediates a continuum between 60S ribosome biogenesis and translation. EMBO Rep. 10, 459–65.CrossRefGoogle ScholarPubMed
Nieuwkoop, P.D. & Faber, J. (1967). Normal table of Xenopus laevis. Daudin. Amsterdam, North Holland.Google Scholar
Reh, T.A. & Kljavin, I.J. (1989). Age of differentiation determines rat retinal germinal cell phenotype: induction of differentiation by dissociation. J. Neurosci. 9, 4179–89.CrossRefGoogle ScholarPubMed
Sanvito, F., Piatti, S., Villa, A., Bossi, M., Lucchini, G., Marchisio, P.C. & Biffo, S. (1999). The beta4 integrin interactor p27(BBP/elF6) is an essential nuclear matrix protein involved in 60S ribosomal subunit assembly. J. Cell. Biol. 144, 823–37.CrossRefGoogle Scholar
Sanvito, F., Vivoli, F., Gambini, S., Santambrogio, G., Catena, M., Viale, E., Veglia, F., Donadini, A., Biffo, S. & Marchisio, P.C. (2000). Expression of a highly conserved protein, p27BBP, during the progression of human colorectal cancer. Cancer Res. 60, 510–16.Google ScholarPubMed
Straznicky, K. & Gaze, R.M. (1971). The growth of the retina in Xenopus laevis: an autoradiographic study. J. Embryol. Exp. Morphol. 26, 6779.Google ScholarPubMed
Vaccaro, M.C., Cuccaro, M., De Marco, N. & Campanella, C. (2006a). Isolation and expression pattern of p27 BBP/eIF6 cDNA in Xenopus laevis embryos. Mol. Reprod. Dev. 73, 485490.Google Scholar
Vaccaro, M.C., Cuccaro, M., De Marco, N. & Campanella, C. (2006b). Isolation and expression pattern of p27 BBP/eIF6 cDNA in Xenopus laevis embryos. ERRATUM Mol. Reprod. Dev. 73, 1612.Google Scholar
Viczian, A.S., Vignali, R., Zuber, M.E., Barsacchi, G. & Harris, W.A. (2003). Xotx5b and Xotx2 regulate photoreceptor and bipolar fates in the Xenopus retina. Development 130, 1281–94.CrossRefGoogle ScholarPubMed
Wetts, R., Serbedzija, G.N. & Fraser, S.E. (1989). Cell lineage analysis reveals multipotent precursors in the ciliary margin of the frog retina. Dev. Biol. 136, 254–63.CrossRefGoogle ScholarPubMed
Yeo, W. & Gautier, J. (2003). A role for programmed cell death during early neurogenesis in Xenopus. Dev. Biol. 260, 3145.CrossRefGoogle ScholarPubMed