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Abstract The proteins Oskar (Osk) in Drosophila and Bucky ball (Buc) in zebrafish act as germ plasm organizers. Both proteins recapitulate germ plasm activities but seem to be unique to their animal groups. Here, we discover that Osk and Buc show similar activities during germ cell specification. Drosophila Osk induces additional PGCs in zebrafish. Surprisingly, Osk and Buc do not show homologous protein motifs that would explain their related function. Nonetheless, we detect that both proteins contain stretches of intrinsically disordered regions (IDRs), which seem to be involved in protein aggregation. IDRs are known to rapidly change their sequence during evolution, which might obscure biochemical interaction motifs.
Indeed, we show that Buc binds to the known Oskar interactors Vasa protein and nanos mRNA indicating conserved biochemical activities. These data provide a molecular framework for two proteins with unrelated sequence but with equivalent function to assemble a conserved core-complex nucleating germ plasm.
Author summary Multicellular organisms use gametes for their propagation. Gametes are formed from germ cells, which are specified during embryogenesis in some animals by the inheritance of RNP granules known as germ plasm. Transplantation of germ plasm induces extra germ cells, whereas germ plasm ablation leads to the loss of gametes and sterility. Therefore, germ plasm is key for germ cell formation and reproduction.
However, the molecular mechanisms of germ cell specification by germ plasm in the vertebrate embryo remain an unsolved question. Proteins, which assemble the germ plasm, are known as germ plasm organizers. Here, we show that the two germ plasm organizers Oskar from the fly and Bucky ball from the fish show similar functions by using a cross species approach. Both are intrinsically disordered proteins, which rapidly changed their sequence during evolution. Moreover, both proteins still interact with conserved components of the germ cell specification pathway. These data might provide a first example of two proteins with the same biological role, but distinct sequence.
Introduction Living systems have the unique ability to reproduce copies of themselves. In animals, the reproductive cells or their precursors, the primordial germ cells (PGCs) are specified by two different modes during embryogenesis [reviewed in ]. In the inductive mode, the embryo generates signals, which specify a subset of cells to differentiate into PGCs.
This was initially described for mouse and axolotl, which seems to be the ancestral mode [reviewed in ]. In the alternative, maternal-inheritance mode, the mother deposits a cytoplasmic determinant termed germ plasm into the oocyte [reviewed in, ].
After fertilization, germ plasm is inherited by a subset of embryonic cells, which then differentiate into PGCs as shown for example in Drosophila, C. Elegans, Xenopus, and zebrafish. Ablation and transplantation experiments demonstrated that germ plasm is necessary and sufficient for PGC specification [reviewed in,, ]. Germ plasm activities can be triggered by a single Drosophila protein termed Oskar (Osk) [reviewed in ]. The steve harvey talk show. Osk mutants fail to assemble germ plasm [, ], whereas mis-localization of Osk induces ectopic PGCs [, ]. Structural and biochemical studies revealed that Osk binds RNA and more recently, that it increases the helicase activity of its interaction partner Vasa [–].