Maternal<i>macho-1</i>is an intrinsic factor that makes cell response to the same FGF signal differ between mesenchyme and notochord induction in ascidian embryos

Kobayashi, Kenji; Sawada, Kaichiro; Yamamoto, Hiroki; Wada, Shinpei; Saiga, Hidetoshi; Nishida, Hiroki

doi:10.1242/dev.00732

Cited by 56 publications

(58 citation statements)

References 46 publications

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“…Using our sensor assay, we demonstrate that miR-124 can downregulate genes from all of these signaling pathways and show that, in several cases, this regulation is conserved in other species. We also show that miR-124 regulates a number of non-neuronal gene targets, including the muscle-specification factor Macho-1 (Kobayashi et al, 2003;Nishida and Sawada, 2001) and numerous Brachyury-regulated genes expressed in the notochord (Corbo et al, 1997;Takahashi et al, 1999). These targets reveal a potential role for miR-124 in the cell lineage specification of the nervous system.…”

mentioning

confidence: 52%

“…In ascidians, Macho-1 is a potent specifier of muscle tissue and Macho-1 mRNA is localized to the most posterior B-line vegetal cells at the 64-cell stage (Kobayashi et al, 2003). Experiments have shown that when Macho-1 is ectopically present in the anterior embryo, the cells that would normally give rise to the CNS are instead converted into muscle (Nishida and Sawada, 2001).…”

Section: Mir-124 Regulates Macho-1 and Many Brachyuryregulated Notochmentioning

confidence: 99%

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miR-124 function during Ciona intestinalis neuronal development includes extensive interaction with the Notch signaling pathway

2011

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SUMMARYThe nervous system-enriched microRNA miR-124 is necessary for proper nervous system development, although the mechanism remains poorly understood. Here, through a comprehensive analysis of miR-124 and its gene targets, we demonstrate that, in the chordate ascidian Ciona intestinalis, miR-124 plays an extensive role in promoting nervous system development. We discovered that feedback interaction between miR-124 and Notch signaling regulates the epidermal-peripheral nervous system (PNS) fate choice in tail midline cells. Notch signaling silences miR-124 in epidermal midline cells, whereas in PNS midline cells miR-124 silences Notch, Neuralized and all three Ciona Hairy/Enhancer-of-Split genes. Furthermore, ectopic expression of miR-124 is sufficient to convert epidermal midline cells into PNS neurons, consistent with a role in modulating Notch signaling. More broadly, genome-wide target extraction with validation using an in vivo tissue-specific sensor assay indicates that miR-124 shapes neuronal progenitor fields by downregulating non-neural genes, notably the muscle specifier Macho-1 and 50 Brachyuryregulated notochord genes, as well as several anti-neural factors including SCP1 and PTBP1. 3ЈUTR conservation analysis reveals that miR-124 targeting of SCP1 is likely to have arisen as a shared, derived trait in the vertebrate/tunicate ancestor and targeting of PTBP1 is conserved among bilaterians except for ecdysozoans, while extensive Notch pathway targeting appears to be Ciona specific. Altogether, our results provide a comprehensive insight into the specific mechanisms by which miR-124 promotes neuronal development.

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mentioning

confidence: 52%

Section: Mir-124 Regulates Macho-1 and Many Brachyuryregulated Notochmentioning

confidence: 99%

miR-124 function during Ciona intestinalis neuronal development includes extensive interaction with the Notch signaling pathway

2011

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“…The identification of Macho-1 as a maternal determinant of posterior vegetal fates (Nishida and Sawada, 2001;Kobayashi et al, 2003) gave cues to understand axial patterning of this chordate embryo for the mesendodermal fates. An anteroposterior difference also exists between the two ectodermal lineages (a-and b-lines) from the eight-cell stage (Rose, 1939;Reverberi and Minganti, 1947;Okado and Takahashi, 1990;Hudson and Lemaire, 2001).…”

Section: Introductionmentioning

confidence: 99%

Ci-FoxA-ais the earliest zygotic determinant of the ascidian anterior ectoderm and directly activatesCi-sFRP1/5

et al. 2006

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This work focuses on the anteroposterior patterning of the ectoderm in the invertebrate chordate Ciona intestinalis. Previous work indicated that, by the eight-cell stage, the anterior and posterior animal blastomeres have acquired different properties, including a differential responsiveness to inducing signals from the underlying mesendoderm. Here, we investigated the molecular basis of this distinction. For this, we studied the regulation of the earliest marker specific for the anterior ectoderm, Ci-sFRP1/5, which is activated at the 64-cell stage. We first found that the activation of this marker in the anterior ectoderm does not involve communication with other lineages. We then identified, by phylogenetic footprinting and deletion analysis, a short conserved minimal enhancer driving the onset of expression of Ci-sFRP1/5. We showed that this enhancer was a direct target of the Ci-FoxA-a gene, a FoxA/HNF3 orthologue expressed in anterior ectodermal and mesendodermal lineages from the eight-cell stage. Gain-and loss-of-function experiments revealed that Ci-FoxA-a is necessary and sufficient within the ectoderm to impose an ectodermal anterior identity, and to repress the posterior programme. Thus, Ci-FoxA-a constitutes a major early zygotic anterior determinant for the ascidian ectoderm, acting autonomously in this territory, prior to the onset of vegetal inductions. Interestingly, while vertebrate FoxA2 are also involved in the regionalization of the ectoderm, they are thought to act during gastrulation to control, in the mesendoderm, the expression of organizer signals. We discuss the evolution of chordate ectodermal patterning in light of our findings.

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“…When PVC is removed from eggs, mirror-image duplication of the anterior half occurs in the cell fates and cleavage pattern. Muscle and mesenchyme precursor blastomeres are converted to nerve cord and notochord, respectively, so that central endoderm blastomeres are encircled by these blastomeres (Nishida, 1994;Kobayashi et al, 2003). The transplantation of the PVC to the anterior Maternal mRNAs localized to specific regions in eggs play important roles in the establishment of embryonic axes and germ layers in various species.…”

Section: Introductionmentioning

confidence: 99%

POPK-1/Sad-1 kinase is required for the proper translocation of maternal mRNAs and putative germ plasm at the posterior pole of the ascidian embryo

2005

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Maternal mRNAs localized to specific regions in eggs play important roles in the establishment of embryonic axes and germ layers in various species. Type I postplasmic/PEM mRNAs, which are localized to the posterior-vegetal cortex (PVC) of fertilized ascidian eggs, such as the muscle determinant macho-1 mRNA, play key roles in embryonic development. In the present study, we analyzed the function of the postplasmic/PEMRNA Hr-POPK-1, which encodes a kinase of Halocynthia roretzi. When the function of POPK-1 was suppressed by morpholino antisense oligonucleotides, the resulting malformed larvae did not form muscle or mesenchyme, as in macho-1-deficient embryos. Epistatic analysis indicated that POPK-1 acts upstream of macho-1. When POPK-1was knocked down, localization of every Type I postplasmic/PEM mRNA examined, including macho-1, was perturbed, showing diffuse early distribution and eventual concentration into a smaller area. This is the probable reason for the macho-1 dysfunction. The postplasmic/PEMmRNAs such as macho-1 and Hr-PEM1 are co-localized with the cortical endoplasmic reticulum (cER) and move with it after fertilization. Eventually they become highly concentrated into a subcellular structure, the centrosome-attracting body (CAB), at the posterior pole of the cleaving embryos. The suppression of POPK-1 function reduced the size of the domain of concentrated cER at the posterior pole, indicating that POPK-1 is involved in the movement of postplasmic/PEM RNAs via relocalization of cER. The CAB also shrank. These results suggest that Hr-POPK-1 plays roles in concentration and positioning of the cER, as well as in the concentration of CAB materials, such as putative germ plasm, in the posterior blastomeres.

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Maternalmacho-1is an intrinsic factor that makes cell response to the same FGF signal differ between mesenchyme and notochord induction in ascidian embryos

Abstract: SummaryMaternal macho-1 is an intrinsic factor that makes cell response to the same FGF signal differ between mesenchyme and notochord induction in ascidian embryos

Cited by 56 publications

References 46 publications

miR-124 function during Ciona intestinalis neuronal development includes extensive interaction with the Notch signaling pathway

miR-124 function during Ciona intestinalis neuronal development includes extensive interaction with the Notch signaling pathway

Ci-FoxA-ais the earliest zygotic determinant of the ascidian anterior ectoderm and directly activatesCi-sFRP1/5

POPK-1/Sad-1 kinase is required for the proper translocation of maternal mRNAs and putative germ plasm at the posterior pole of the ascidian embryo

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