Chromatin Decondensation and Nuclear Reprogramming by Nucleoplasmin

Tamada, Hiroshi; Thuan, Nguyen Van; Reed, Peter; Nelson, Dominic; Katoku-Kikyo, Nobuko; Wudel, Justin; Wakayama, Teruhiko; Kikyo, Nobuaki

doi:10.1128/mcb.01302-07

Cited by 37 publications

(59 citation statements)

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“…From these data, it can be concluded that Cag-nucleophosmin and Ca-nucleophosmin are associated with keeping chromosomes in a state of decondensation not only in male pronucleus formation but in spermatogonia storage as well. This is consistent with the function of nucleoplasmin in undifferentiated mouse cells (Tamada et al 2006). In previous reports, all in vitro sperm decondensation systems have used either Xenopus nucleoplasmin (Iwata et al 1999) or Xenopus sperm (Crevel et al 1997;Kawasaki et al 1994).…”

Section: Discussionsupporting

confidence: 82%

Molecular Characterization and Functional Commonality of Nucleophosmin/Nucleoplasmin in Two Cyprinid Fish

Gui

2009

Biochem Genet

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Nucleophosmin/nucleoplasmin has been studied mostly in mammals and amphibians. To clarify the characteristics and function of nucleophosmin/ nucleoplasmin in teleost fish, we cloned a full-length cDNA sequence from two cyprinid fish, Carassius auratus gibelio and Carassius auratus. Molecular characterization and multiple sequence alignments suggested that they are the homologs of nucleophosmin. RT-PCR and Western blot detected a specific expression in gonads, and immunofluorescence localization revealed their distribution in oogenic and spermatogenic cells. Furthermore, a sperm decondensation function was demonstrated by immunodepletion and in vitro sperm decondensation experiments. The data suggest that the cloned nucleophosmin should share expressional and functional characterization with nucleoplasmin and therefore provide novel evidence for a functional commonality of nucleophosmin and nucleoplasmin in fish.

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Section: Discussionsupporting

confidence: 82%

Molecular Characterization and Functional Commonality of Nucleophosmin/Nucleoplasmin in Two Cyprinid Fish

Gui

2009

Biochem Genet

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“…Indeed, the decondensation of chromatin is followed by an increase in transcriptio n, as measured by active polymerase II loading, bromine-labelled UTP (BrUTP) incorporation or histone H3 trimethylation on Lys4 (H3K4me3), and these changes are seen in almost all nuclei transplanted into oocytes 18,23 . Nucleoplasmin-mediated decondensation of nuclei before ooc-NT improves gene reactivation, demonstrating the importance of this process for successful transcriptional reprogramming 21 . Similarly, chromatin decondensation precedes gene reactivation following cell fusion 20 .…”

Section: Early Morphological Changesmentioning

confidence: 97%

“…This change is reminiscent of what happens to sperm chromatin at fertilization. Chromatin decondensation seems to be a hallmark of reprogramming, as it is observed following nuclear transfer to eggs 17 and oocytes 18 , in cell fusion experiments 19,20 , and in somatic nuclei exposed to egg extract 21 .…”

Section: Early Morphological Changesmentioning

confidence: 99%

Mechanisms of nuclear reprogramming by eggs and oocytes: a deterministic process?

Jullien

Pasque²,

Halley-Stott³

et al. 2011

Nat Rev Mol Cell Biol

105

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Differentiated cells can be experimentally reprogrammed back to pluripotency by nuclear transfer, cell fusion or induced pluripotent stem cell technology. Nuclear transfer and cell fusion can lead to efficient reprogramming of gene expression. The egg and oocyte reprogramming process includes the exchange of somatic proteins for oocyte proteins, the post-translational modification of histones and the demethylation of DNA. These events occur in an ordered manner and on a defined timescale, indicating that reprogramming by nuclear transfer and by cell fusion rely on deterministic processes.The remarkable stability of cell differentiation under normal conditions can be reversed experimentally by nuclear transfer, cell fusion and induced pluripotent stem (iPS) cell technology [1][2][3][4][5] . This provides an opportunity to generate pluripotent embryonic cells from adult cells of the same individual and hence opens the possibilit y of cell replacement without the need for immunosuppression.iPS cell technology makes use of the overexpression of transcription factors (FIG. 1a) and has been extensively reviewed, so it is not discussed in detail [6][7][8][9] . To generate entirely unrelated cell types by iPS cell technology, treated cells must be grown for multiple cell divisions over a long period of time (up to 3 weeks). By contrast, nuclear transfer and cell fusion do not involve the overexpression of new genes, and instead make use of natura components present in eggs and some early embryos to initiate new transcription.There are two kinds of nuclear transfer experiments: egg-NT involves the transfer of a single somatic nucleus to an unfertilize d enucleated egg (in both mammals and amphibians) 1 (FIG. 1b); and ooc-NT involves the transplantation of multiple somatic cell nuclei into the germinal vesicle (the nucleus) of a growing meiotic prophase amphibian oocyte (an immature egg) 10 (FIG. 1c). Note that the terms egg and oocyte refer to different developmental stages in amphibians and mammals: amphibian eggs are in metaphase II of meiosis, which is equivalent to mouse metaphase II stage oocytes, whereas their immediate precursors, oocytes, are blocked in meiotic prophase I, which is equivalent to mouse germinal vesicle stage oocytes.© 2011 Macmillan Publishers Limited. All rights reserved Correspondence to J.B.G.j.gurdon@gurdon.cam.ac.uk. Competing interests statementThe authors declare no competing financial interests. There are important differences between the two types of nuclear transfer experimen t. Extensive cell division takes place in egg-NT experiments, and functional new cell types appear as the nuclear transplant embryo develops. By contrast, in ooc-NT experiments, no new cell types are formed, and neither the oocyte nor the introduced nuclei divide, but there is a direct transition from nuclei of differentiated cells to reprogrammed nuclei that transcribe pluripotency genes. Analysis of the mechanism of reprogramming (which involves transcription of pluripotency and other genes) in egg-NT expe...

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“…These include ISWI (10), FRGY2a/b (11), BRG1 (12), Nucleoplasmin (13), and Histone B4 (14). Although the roles of these factors on nuclear remodeling and transcriptional reprogramming have been shown, it has not been demonstrated that these factors are crucial for nuclear reprogramming in NT embryos during embryonic development.…”

mentioning

confidence: 99%

“…We focused on protein exchange in extract-treated nuclei because the exchange of nuclear proteins between a donor nucleus and an oocyte cytoplasm is a prominent phenomenon during reprogramming (18)(19)(20). Additionally, some proteins, such as ISWI and nucleoplasmin, that are incorporated from Xenopus egg extracts into donor nuclei have been shown to have a role in reprogramming (10,13). After incubation of somatic nuclei in oocyte extracts, proteins that become associated with somatic nuclei from the extracts were identified by mass spectrometry.…”

mentioning

confidence: 99%

Identification and characterization of an oocyte factor required for development of porcine nuclear transfer embryos

Miyamoto

Nagai²,

Kitamura³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Nuclear reprogramming of differentiated cells can be induced by oocyte factors. Despite numerous attempts, these factors and mechanisms responsible for successful reprogramming remain elusive. Here, we identify one such factor, necessary for the development of nuclear transfer embryos, using porcine oocyte extracts in which some reprogramming events are recapitulated. After incubating somatic nuclei in oocyte extracts from the metaphase II stage, the oocyte proteins that were specifically and abundantly incorporated into the nuclei were identified by mass spectrometry. Among 25 identified proteins, we especially focused on a multifunctional protein, DJ-1. DJ-1 is present at a high concentration in oocytes from the germinal vesicle stage until embryos at the fourcell stage. Inhibition of DJ-1 function compromises the development of nuclear transfer embryos but not that of fertilized embryos. Microarray analysis of nuclear transfer embryos in which DJ-1 function is inhibited shows perturbed expression of P53 pathway components. In addition, embryonic arrest of nuclear transfer embryos injected with anti-DJ-1 antibody is rescued by P53 inhibition. We conclude that DJ-1 is an oocyte factor that is required for development of nuclear transfer embryos. This study presents a means for identifying natural reprogramming factors in mammalian oocytes and a unique insight into the mechanisms underlying reprogramming by nuclear transfer.oocyte extract and proteomics | reprogramming in mammalian oocytes E mbryonic cells differentiate into specific types of cells as development progresses. Once differentiated, the reversion of a differentiated cell state to an original undifferentiated state is strictly inhibited in normal development. However, it has been experimentally shown that differentiated nuclei can be returned to an undifferentiated embryonic state after nuclear transfer (NT) to enucleated eggs or oocytes (1, 2). Such experiments provide an opportunity to reprogram somatic cells as a means to prepare undifferentiated cells, which may be differentiated into any kinds of cells for cell-replacement therapy. Recently, nuclear reprogramming technology has been expanded by the production of induced pluripotent stem (iPS) cells (3). iPS cells can be obtained by overexpressing specific sets of transcription factors such as Oct4, Sox2, Klf4, and c-myc in cultured cells. The processes leading to establishment of iPS cell lines are being carefully examined and we are begining to understand how somatic cells acquire pluripotency by this method (4-6). The mechanisms leading to pluripotency may be different between iPS cells and NT embryos because somatic nuclei transferred into unfertilized metaphase II (MII) oocytes must undergo early embryonic development before the inner cell mass (ICM) can give rise to pluripotent embryonic stem (ES) cells. In addition, the molecules and mechanisms that induce somatic cell reprogramming are expected to be different between iPS cells and NT embryos (7,8). A recent study has shown that nuclear t...

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Chromatin Decondensation and Nuclear Reprogramming by Nucleoplasmin

Cited by 37 publications

References 0 publications

Molecular Characterization and Functional Commonality of Nucleophosmin/Nucleoplasmin in Two Cyprinid Fish

Molecular Characterization and Functional Commonality of Nucleophosmin/Nucleoplasmin in Two Cyprinid Fish

Mechanisms of nuclear reprogramming by eggs and oocytes: a deterministic process?

Identification and characterization of an oocyte factor required for development of porcine nuclear transfer embryos

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