Ringo/Cyclin-dependent Kinase and Mitogen-activated Protein Kinase Signaling Pathways Regulate the Activity of the Cell Fate Determinant Musashi to Promote Cell Cycle Re-entry in Xenopus Oocytes

Arumugam, Karthik; MacNicol, Melanie C.; Wang, Yiying; Cragle, Chad E.; Tackett, Alan J.; Hardy, Linda; MacNicol, Angus M.

doi:10.1074/jbc.m111.300681

Cited by 31 publications

(64 citation statements)

References 48 publications

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“…In this context, PARN is thought to exert a dominant effect and thereby override GLD2 activity to maintain short poly(A) tails and translational dormancy. Upon progesterone stimulation, CPEB1 undergoes phosphorylation of Ser-174, which triggers expulsion of PARN from the complex and leads to the unopposed action of GLD2 and consequent extension of poly(A) tails of CPE-regulated mRNAs (23). We see a similar co-association of Musashi with both GLD2 and PARN in immature oocytes.…”

Section: Discussionsupporting

confidence: 59%

mentioning

confidence: 99%

“…Ringo then activates free cyclin-dependent kinase subunits, triggering phosphorylation of several targets, including Musashi (23). Musashi phosphorylation triggers the cytoplasmic polyadenylation and translation of several target mRNAs, including those encoding Mos, cyclin B5, and Nrp1A/B (Musashi-1) prior to GVBD (10,(23)(24)(25). Subsequently, Mosdependent activation of MAPK signaling primes CPEB1 for activation (26), leading to de-repression and translational activation of CPE-dependent mRNAs, including those encoding cyclin B1, Wee1, and CPEB4 (27)(28)(29)(30).…”

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confidence: 99%

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Musashi Protein-directed Translational Activation of Target mRNAs Is Mediated by the Poly(A) Polymerase, Germ Line Development Defective-2

Cragle¹,

MacNicol

2014

Journal of Biological Chemistry

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Section: Discussionsupporting

confidence: 59%

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confidence: 99%

mentioning

confidence: 99%

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Musashi Protein-directed Translational Activation of Target mRNAs Is Mediated by the Poly(A) Polymerase, Germ Line Development Defective-2

Cragle¹,

MacNicol

2014

Journal of Biological Chemistry

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“…mRNAs containing MBEs are bound by the Musashi protein, contain short poly(A) tails, and are translationally repressed in oocytes by an unknown mechanism. In response to progesterone and oocyte maturation, Musashi is phosphorylated, and the protein directs the polyadenylation of MBE-containing mRNAs, through the recruitment and/or activation of a poly(A) polymerase (Cragle and MacNicol 2014b; Arumugam et al 2012). …”

Section: 5 Translational Control Mechanisms Operating During Xenopumentioning

confidence: 99%

Controlling the Messenger: Regulated Translation of Maternal mRNAs in Xenopus laevis Development

Sheets

Fox

Dowdle

et al. 2016

Advances in Experimental Medicine and Biology

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The selective translation of maternal mRNAs encoding cell-fate determinants drives the earliest decisions of embryogenesis that establish the vertebrate body plan. This chapter will discuss studies in Xenopus laevis that provide insights into mechanisms underlying this translational control. Xenopus has been a powerful model organism for many discoveries relevant to the translational control of maternal mRNAs because of the large size of its oocytes and eggs that allow for microinjection of molecules and the relative ease of manipulating the oocyte to egg transition (maturation) and fertilization in culture. Consequently, many key studies have focused on the expression of maternal mRNAs during the oocyte to egg transition (the meiotic cell cycle) and the rapid cell divisions immediately following fertilization. This research has made seminal contributions to our understanding of translational regulatory mechanisms, but while some of the mRNAs under consideration at these stages encode cell-fate determinants, many encode cell cycle regulatory proteins that drive these early cell cycles. In contrast, while maternal mRNAs encoding key developmental (i.e., cell-fate) regulators that function after the first cleavage stages may exploit aspects of these foundational mechanisms, studies reveal that these mRNAs must also rely on distinct and, as of yet, incompletely understood mechanisms. These findings are logical because the functions of such developmental regulatory proteins have requirements distinct from cell cycle regulators, including becoming relevant only after fertilization and then only in specific cells of the embryo. Indeed, key maternal cell-fate determinants must be made available in exquisitely precise amounts (usually low), only at specific times and in specific cells during embryogenesis. To provide an appreciation for the regulation of maternal cell-fate determinant expression, an overview of the maternal phase of Xenopus embryogenesis will be presented. This section will be followed by a review of translational mechanisms operating in oocytes, eggs, and early cleavage-stage embryos and conclude with a discussion of how the regulation of key maternal cell-fate determinants at the level of translation functions in Xenopus embryogenesis. A key theme is that the molecular asymmetries critical for forming the body axes are established and further elaborated upon by the selective temporal and spatial regulation of maternal mRNA translation.

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“…The presence of Musashi protein in immature stage VI oocytes suggested that Musashi must undergo a functional switch in response to progesterone to promote MBE-dependent early class polyadenylation and translational activation. Phosphorylation of Musashi1 is initially dependent upon Ringo/CDK activity and is subsequently augmented by MAP kinase signaling (Arumugam et al 2012b). Mutational disruption of these sites abrogates the ability of Musashi1 to mediate MBEdependent polyadenylation and translational activation.…”

Section: Cpe-independent Mrna Translational Regulationmentioning

confidence: 99%

From Oocyte to Fertilizable Egg

Cragle

MacNicol

2014

Xenopus Development

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The primary point of regulation in control of messenger RNA (mRNA) translation occurs at initiation. Assembly of a functional ribosome onto an mRNA is a complex, multistep process. Two important regulated steps include the binding and formation of the 5′ cap complex, eIF4F, and recruitment of the small ribosomal subunit as part of a 43S preinitiation complex (Figure 3.1). Formation of both the cap complex and the preinitiation complex, specifically the ternary complex (the initiator methionine-charged tRNA i , the Abstract: Growing evidence indicates a critical role for posttranscriptional mechanisms for regulation of gene expression in a variety of developmental transitions as well as for control of adult somatic cell function. A predominant regulatory paradigm is selective control of messenger RNA (mRNA) translation. Significant advances have provided unparalleled insight into the diverse mRNA translational control processes that govern early development and cell cycle progression. At the forefront of these new insights is work analyzing oocyte maturation in the frog Xenopus laevis. We will review general concepts underlying mRNA translational regulation and highlight recent advances characterizing RNA binding proteins (RBP) and their target sequences in the control of oocyte growth and maturation. In particular, we will discuss the characterization of bifunctional elements, which can switch from repression to activation in response to changes in cellular signaling. We will consider the increasing number of mRNA 3′ untranslated regions (UTRs) containing multiple distinct elements with unique properties and the emerging issue of understanding the functional integration of translational control mechanisms. Finally, we will discuss the elucidation of nested feedback loops that drive and regulate sequential maternal mRNA translational control programs. These new advances indicate that regulated mRNA translation is likely to be much more complex than originally anticipated. The Xenopus oocyte is proving invaluable in the search for common underlying principles that guide mRNA translational control, that are applicable not only to oogenesis and maturation, but also to control of gene expression in somatic cells.

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Ringo/Cyclin-dependent Kinase and Mitogen-activated Protein Kinase Signaling Pathways Regulate the Activity of the Cell Fate Determinant Musashi to Promote Cell Cycle Re-entry in Xenopus Oocytes

Cited by 31 publications

References 48 publications

Musashi Protein-directed Translational Activation of Target mRNAs Is Mediated by the Poly(A) Polymerase, Germ Line Development Defective-2

Musashi Protein-directed Translational Activation of Target mRNAs Is Mediated by the Poly(A) Polymerase, Germ Line Development Defective-2

Controlling the Messenger: Regulated Translation of Maternal mRNAs in Xenopus laevis Development

From Oocyte to Fertilizable Egg

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