A Tribute to the Xenopus laevis Oocyte and Egg

Brown, Donald D.

doi:10.1074/jbc.x400008200

Cited by 46 publications

(42 citation statements)

References 73 publications

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“…In contrast, the 5S rRNA variant expressed in somatic tissues, called somatic-type, just consists of 400 rDNA genes. Thus this oocyte-variant probably evolved to enable the production of the enormous amount of 5S rRNA in oocytes equivalent to that of hundreds of thousands of somatic cells (Brown 2004). Recently, we reported similar 5S rRNA variants in zebrafish (Locati et al 2017), in which a maternaltype 5S r|RNA (2330 genes on chromosome 4) makes up virtually all oocyte 5S rRNA, which is completely replaced during embryogenesis by the somatic-type (12 genes on chromosome 18).…”

Section: Introductionmentioning

confidence: 85%

Expression of distinct maternal and somatic 5.8S, 18S, and 28S rRNA types during zebrafish development

Locati

Pagano

Girard

et al. 2017

RNA

127

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There is mounting evidence that the ribosome is not a static translation machinery, but a cell-specific, adaptive system. Ribosomal variations have mostly been studied at the protein level, even though the essential transcriptional functions are primarily performed by rRNAs. At the RNA level, oocyte-specific 5S rRNAs are long known for Xenopus. Recently, we described for zebrafish a similar system in which the sole maternal-type 5S rRNA present in eggs is replaced completely during embryonic development by a somatic-type. Here, we report the discovery of an analogous system for the 45S rDNA elements: 5.8S, 18S, and 28S. The maternal-type 5.8S, 18S, and 28S rRNA sequences differ substantially from those of the somatic-type, plus the maternal-type rRNAs are also replaced by the somatic-type rRNAs during embryogenesis. We discuss the structural and functional implications of the observed sequence differences with respect to the translational functions of the 5.8S, 18S, and 28S rRNA elements. Finally, in silico evidence suggests that expansion segments (ES) in 18S rRNA, previously implicated in ribosome-mRNA interaction, may have a preference for interacting with specific mRNA genes. Taken together, our findings indicate that two distinct types of ribosomes exist in zebrafish during development, each likely conducting the translation machinery in a unique way.

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Section: Introductionmentioning

confidence: 85%

Expression of distinct maternal and somatic 5.8S, 18S, and 28S rRNA types during zebrafish development

Locati

Pagano

Girard

et al. 2017

RNA

127

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“…Xenopus oocytes have long been used to express injected mRNAs from a wide variety of sources, including viruses (Brown, 2004). Therefore, in experiments addressing the function of nanos1, we were surprised to find that although nanos1 RNA was translated in reticulocyte lysates, it was poorly translated, if at all, after injection into oocytes (Fig.…”

Section: Nanos1 Rna Is Poorly Translated After Injection Into Oocytesmentioning

confidence: 99%

Xenopusgermlinenanos1is translationally repressed by a novel structure-based mechanism

Luo

Nerlick

et al. 2011

Development

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SUMMARYThe translational repressor Nanos is expressed in the germline and stem cell populations of jellyfish as well as humans. Surprisingly, we observed that unlike other mRNAs, synthetic nanos1 RNA translates very poorly if at all after injection into Xenopus oocytes. The current model of simple sequestration of nanos1 within germinal granules is insufficient to explain this observation and suggests that a second level of repression must be operating. We find that an RNA secondary structural element immediately downstream of the AUG start site is both necessary and sufficient to prevent ribosome scanning in the absence of a repressor. Accordingly, repression is relieved by small in-frame insertions before this secondary structure, or translational control element (TCE), that provide the 15 nucleotides required for ribosome entry. nanos1 is translated shortly after fertilization, pointing to the existence of a developmentally regulated activator. Oocyte extracts were rendered fully competent for nanos1 translation after the addition of a small amount of embryo extract, confirming the presence of an activator. Misexpression of Nanos1 in oocytes from unlocalized RNA results in abnormal development, highlighting the importance of TCE-mediated translational repression. Although found in prokaryotes, steric hindrance as a mechanism for negatively regulating translation is novel for a eukaryotic RNA. These observations unravel a new mode of nanos1 regulation at the post-transcriptional level that is essential for normal development.

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“…He and Max Birnstiel were the first to purify a single type of gene in eukaryotes (Brown 1994, Wallace & Birnstiel 1966, well before the era of DNA cloning in bacteria. Brown's work on Xenopus 5S genes continued to lead the way in the molecular biology of development for another two decades (Brown 1982(Brown , 2004. He was aware of the Xenopus O-nu mutation referred to above and showed surprisingly that this mutation involved a complete lack of 18S + 28S ribosomal RNA synthesis, the O-nu tadpoles developing entirely normally for several days by using their maternal inheritance of ribosomes (and their newly synthesized mRNA) (Brown & Gurdon 1964).…”

Section: Oxford Zoology and Caltechmentioning

confidence: 99%

From Nuclear Transfer to Nuclear Reprogramming: The Reversal of Cell Differentiation

Gurdon

2006

Annu. Rev. Cell Dev. Biol.

138

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This is a personal historical account of events leading from the earliest success in vertebrate nuclear transfer to the current hope that nuclear reprogramming may facilitate cell replacement therapy. Early morphological evidence in Amphibia for the toti-or multipotentiality of some nuclei from differentiated cells first established the principle of the conservation of the genome during cell differentiation. Molecular markers show that many somatic cell nuclei are reprogrammed to an embryonic pattern of gene expression soon after nuclear transplantation to eggs. The germinal vesicles of oocytes in first meiotic prophase have a direct reprogramming activity on mammalian as well as amphibian nuclei and offer a route to identify nuclear reprogramming molecules. Amphibian eggs and oocytes have a truly remarkable ability to transcribe genes as DNA or nuclei, to translate mRNA, and to modify or localize proteins injected into them. The development of nuclear transplant embryos depends on the ability of cells to interpret small concentration changes of signal factors in the community effect and in morphogen gradients. Many difficulties in a career can be overcome by analyzing in increasing depth the same fundamentally interesting and important problem.

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A Tribute to the Xenopus laevis Oocyte and Egg

Cited by 46 publications

References 73 publications

Expression of distinct maternal and somatic 5.8S, 18S, and 28S rRNA types during zebrafish development

Expression of distinct maternal and somatic 5.8S, 18S, and 28S rRNA types during zebrafish development

Xenopusgermlinenanos1is translationally repressed by a novel structure-based mechanism

From Nuclear Transfer to Nuclear Reprogramming: The Reversal of Cell Differentiation

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