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The latter distribution would imply a target of localization that is distinct from all other vegetally localized transcripts. After fertilization, the B7 transcripts disappear, the Xlsirt , Xcat-2 , and Xcat-3 transcripts are associated with the germ plasm in the primordial germ cells, and the other transcripts B9, B12, C10 , Vg1 , Xcat-4 , and Xwnt are all located in the vegetal blastomeres 70 , 79 , 90 , 93 , 98 , 99 ; L Etkin, personal communication.

During maturation, PCNA mRNA becomes concentrated in the central ectoplasm and cortical regions surrounding the myoplasm but is absent from the myoplasm per se While PCNA mRNA can be observed in both the ectoplasm and the myoplasm after the first phase of ooplasmic segregation, which restricts the ectoplasm and myoplasm to the vegetal hemisphere, PCNA mRNA is absent from the myoplasm in the two-cell embryo YC RNA is distributed throughout the cytoplasm of previtellogenic oocytes However, during early vitellogenesis, YC transcripts are localized around the nucleus.

They gradually move away from the nucleus as the oocyte increases in size, until they become restricted to the cortex of postvitellogenic oocytes After the first phase of ooplasmic segregation shortly after fertilization, YC transcripts are localized in the vegetal cap of myoplasm A third pattern of localization is exhibited by L5 transcripts, which are concentrated in the cortical myoplasm except at the animal pole during oogenesis After fertilization, L5 transcripts become restricted to the vegetal myoplasm There is one example of a maternally synthesized mRNA that is localized in the echinoderm Strongylocentrotus purpuratus oocyte and early embryo Since there are no markers of the animal-vegetal axis of the egg, the location of SpCOUP-TF transcripts in the egg was inferred from their distribution in cleavage stage embryos where the animal-vegetal and oral-aboral axes are evident morphologically.

From this inference it was concluded that SpCOUP-TF transcripts are localized such that they are restricted to one of the two cells produced by the first cleavage i. There is one example of a maternally synthesized mRNA that is localized within the cells of the zebrafish Brachydanio rerio embryo Maternally synthesized zebrafish vasa transcripts localize to the inner yolk-most edges of the cleavage furrows at the first embryonic cell division This localization pattern is maintained through the four-cell stage. From the 8- to the cell stage, the vasa transcripts remain in only four cells the presumptive primordial germ cells and are found in intracellular clumps that likely represent the assembling germ plasm.

Subsequently, vasa transcripts are found in all primordial germ cells and germ cells. Many cells in addition to oocytes are polarized. Epithelial cells have an apical-basal polarity. Differentiated neurons have dendritic arbors and an axon. Fibroblasts have specialized moving membranes lamellopodia at defined surfaces. These classes of cells also show asymmetric distributions of RNAs. However, in most cases, the developmental significance of RNA localization is unknown or, alternatively, transcript localization serves a function in the fully differentiated cell rather than during its development or differentiation.

Several RNA localization patterns in these polarized cells are described here. Although neurons can exhibit very complex and quite varied cytoarchitectures, they are classic examples of polarized cells and generally have an axon on one side of the cell body soma and dendrites on the other. Most neuronal RNAs are present only in the soma and are excluded from dendrites and axons. At least 12 localized neuronal RNAs have been reported 1 , , These RNAs can be classified into two different patterns. In almost all cases these RNAs are localized in differentiated neurons.

The exception, tropomyosin-5 Tm5 RNA, is localized prior to any structural polarities at the future axonal pole of differentiating neurons In mature neurons Tm5 RNA is present only in the soma Several types of cells have defined areas of membrane devoted to a particular function.

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Apical ends of villar epithelial cells also have high concentrations of actin mRNA In these cases, the distribution of mRNA likely follows the differentiation of these cell types rather than playing a role during their differentiation. In Drosophila the location of plus-end kinesin - and minus-end Nod -directed microtubule motors provides a readout of the polarities of various cell types. Localization of these motors within oocytes was mentioned earlier. In addition, these motors localize to opposite ends of polarized cells 36 : epithelia Nod is apical and kinesin is basal , mitotic spindles Nod is at the poles , neurons Nod is dendritic and kinesin is axonal , and muscle Nod is at the center and kinesin at attachment sites.

As mentioned previously, several mRNAs e. In addition, mRNAs e. It has been reported that prospero and inscuteable mRNAs are localized within embryonic Drosophila neuroblasts The inscuteable transcripts are apically localized during interphase of the neuroblast cell divisions, while prospero transcripts are apically localized at interphase but are basal from prophase to telophase.

Basal prospero RNA is segregated into one daughter cell the ganglion mother cell. The S. This section focuses on general classes of RNA localization mechanisms. Specific details of cis -acting sequences and trans -acting factors that function in RNA localization are reviewed in the following section. An obvious way to achieve cytoplasmic RNA localization is to export transcripts vectorially from only one side of the nucleus and then to transport or anchor them in the cytoplasm on that side of the nucleus. Substantial progress has been made recently in understanding the mechanisms of nucleo-cytoplasmic transport ; however, studies of vectorial aspects of transport from the nucleus are in their infancy.

In general, it has been difficult to establish vectorial nucleo-cytoplasmic transport for particular transcripts due to experimental limitations. An exception is the case of pair-rule gene transcripts hairy and fushi tarazu in the cellularizing blastoderm of Drosophila 65 , Here it was possible to use mutations to produce two layers of nuclei or displaced nuclei in the cortex of the syncytial blastoderm and, thus, to show—for the inner nuclei—that transcripts are vectorially exported even in the absence of normal apical cytoskeletal structures.

The fact that this is possible suggests that the nuclei themselves have a polarity independent of the cytoplasmic cytoskeleton. A second example of vectorial nucleo-cytoplasmic export may be the Drosophila gurken mRNA that is localized dorso-anterior to the nucleus in stage 8 oocytes. The gurken transcripts are synthesized in the oocyte nucleus itself R Cohen, personal communication , and the K10 and Squid proteins may function in vectorial transport of the gurken mRNA see below.

A second class of localization mechanism applies during Drosophila oogenesis. As outlined previously, RNAs are transported from the nurse cells into the oocyte through intercellular bridges known as ring canals. Nurse cells connect only to the presumptive anterior pole of the oocyte, so that the imported RNAs first arrive at the oocyte's anterior pole. It is likely that anteriorly localized RNAs e.

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The fact that mutants in which nurse cells connect to the oocyte at both poles result in bipolar transport into the oocyte and trapping of bicoid RNA at both poles 42 supports this hypothesis. Recent experiments in which so-called localization particles were followed by time-lapse confocal microscopy supports this hypothesis further WE Theurkauf, TI Hazelrigg, personal communication. In contrast to the entrapment seen for anterior-localized RNAs, those that are localized to the posterior pole are actively transported there in association with the cytoskeleton or are localized there by other mechanisms such as degradation-protection see below.

The posterior polar plasm of Drosophila oocytes and early embryos contains large, non-membrane-bound organelles known as polar granules, which are involved in germ cell formation and specification see below. Mitochondria are found in close association with the polar granules. This RNA appears to be exported from the mitochondria into the cytoplasm within the posterior polar plasm and to be associated with polar granules 61 , , , , , Indeed, given the apposition of polar granules and mitochondria, the mtlrRNA may in fact be exported vectorially out of mitochondria directly into or onto the polar granules.

The function of the mtlrRNA in the polar granules is unclear, although it has been implicated in pole cell formation There is some disagreement, however, about whether a high local concentration of mtlrRNA is indeed necessary for pole cell formation , , It was postulated several years ago that one mechanism by which a generalized RNA distribution could be converted to a restricted pattern was through degradation of the RNA throughout the cell except at the site of localization Several Drosophila transcripts represent variants of this type of process.

For example, while the bulk of maternally synthesized nanos and cyclin B transcripts are concentrated in the posterior polar plasm of the early embryo, a subset of these transcripts remains unlocalized 62 , , , The posteriorly localized transcripts are taken up into the pole cells when they bud, while the unlocalized transcripts are degraded 62 , , , There is a close correlation between translational repression of unlocalized nanos transcripts and their degradation reviewed in Under normal conditions, the polar granules are necessary and sufficient for protection of nanos , cyclin B , and Hsp83 transcripts from degradation at the posterior 56 , 60 , During oogenesis the YC RNA is perinuclear, gradually moving to the cortex, and after fertilization the RNA segregates to the myoplasm and associates with the cytoskeleton Asymmetries in cytoskeletal organization have been described earlier for both Xenopus and Drosophila oocytes.

Further, there is colocalization of specific RNAs with either a minus-end-directed microtubule motor Nod or a plus-end-directed motor kinesin , in particular regions of the Drosophila oocyte's cytoplasm see above. There is now substantial evidence that cytoplasmic RNA transport to specific intracellular destinations is accomplished by both the microtubule- and the microfilament-based cytoskeleton. The following section reviews evidence for a role of the cytoskeleton in anchoring localized RNAs at their intracellular destinations.

Here the role of the cytoskeleton in directed cytoplasmic transport is reviewed. Analysis of intracellular transport mechanisms requires the ability to systematically perturb normal cytoskeletal function.

RNA LOCALIZATION IN DEVELOPMENT | Annual Review of Biochemistry

These studies have been aided in Xenopus and Drosophila by drugs that specifically perturb either the microtubule-based colchicine, nocodazole, or taxol or the microfilament-based cytochalasins cytoskeleton. In addition, mutations that affect components of the cytoskeleton have led to informative results in Drosophila and Saccharomyces. Localized RNAs have several characteristic and sequential patterns of expression during Drosophila oogenesis that correlate with particular aspects of the cytoskeleton, particularly the microtubules see above.

Over a dozen transcripts are synthesized in the nurse cells and specifically accumulate in the oocyte within early egg chambers prior to their localization [ bicoid 7 , nanos 28 , orb 23 , oskar 24 , 25 , Add-hts 16 , Bicaudal-C 18 , Bicaudal-D 19 , gurken 21 , Pgc 26 , K10 22 , egalitarian 20 , and tudor 27 ]. Transport of these RNAs into the oocyte is likely to be carried out by minus-end-directed microtubule motors since the MTOC is located in the oocyte during these stages see above.

Although no specific motors have been demonstrated to be involved in this process, the kinesin-like minus-end-directed motor—Nod—localizes first to the oocyte and then to its posterior at the same stages as many of these RNAs are transported into the oocyte and then accumulate at its posterior pole Dynein a minus-end-directed motor is also localized to the oocyte at these stages but does not appear to be involved in RNA transport and localization During these stages, several RNAs are present in detergent insoluble fractions e. Moreover, the association of bicoid , oskar , and Bicaudal-D RNAs with the cytoskeleton is sensitive to colchicine and not to cytochalasins, indicating that microtubules but not microfilaments are involved in their transport and localization 37 , The phenotypes of orb , egalitarian , and Bicaudal-D mutants suggest a role in oocyte specific RNA accumulation.

Egalitarian and Bicaudal-D proteins are made in nurse cells and are transported to the posterior of the oocyte presumably along minus-directed microtubules The distribution of Egalitarian and Bicaudal-D proteins parallels that of the RNAs that are transported into the oocyte at these stages. Microtubule inhibitors result in delocalization of Egalitarian protein Moreover, in egalitarian mutants oskar and orb RNA are no longer associated with the cytoskeleton This indicates that Egalitarian and Bicaudal-D proteins may be involved—directly or indirectly—in transporting localized RNAs along microtubule networks into and to the posterior of the oocyte.

Mutations in genes required for early localization also perturb oocyte polarity; egalitarian and Bicaudal-D mutations cause all 16 cells of the cyst to become polyploid nurse cells; thus oocyte-specific accumulation of transcripts cannot occur because there is no oocyte 20 , Orb is required for oocyte polarity, and in orb mutants, oocytes are located at ectopic positions within the egg chamber In orb mutant oocytes certain RNAs orb , oskar are still localized—albeit at abnormal positions—whereas others are not localized at all Add-hts , Bicaudal-D , K10 It is possible that Orb protein is required to establish microtubule polarity, whereas Egalitarian and Bicaudal-D are necessary for its maintenance.

As described above, the majority of RNAs transported into and localized in the oocyte have in common early transport from the nurse cells stage 1—5 , transient localization to the posterior stage 6 , and subsequent localization to the anterior stages 7—8.

In addition, oskar and Pgc transcripts move back to the posterior pole of the oocyte at stage 9, whereas the bicoid and Add-hts RNAs never show the early posterior localization but are either always anteriorly localized bicoid or are initially localized throughout the cortex and subsequently localize to the anterior Add-hts. These data suggest that a default transport and localization mechanism is carried out by minus-end-directed microtubule motors, and that certain RNAs bicoid , Add-hts , oskar , Pgc initially use this mechanism to enter the oocyte but then engage a different localization machinery.

Since bicoid and oskar RNA transport and localization are best understood and exemplify distinct localization mechanisms, they are discussed below. During its translocation from the nurse cells into the oocyte, it is apically localized within the nurse cells Both apical nurse cell localization and anterior oocyte localization are sensitive to microtubule depolymerizing drugs colchicine, nocodazole, tubulozole C but not to inhibitors of F-actin polymerization cytochalasin D and B Recent evidence suggests that transport of bicoid RNA into the oocyte actually involves several distinct steps that might be mediated by distinct localization mechanisms; for example, two distinct microtubule-dependent steps drive bicoid RNA localization particles within the nurse cell cytoplasm WE Theurkauf, TI Hazelrigg, personal communication , but transport through the ring canals into the oocyte is resistant to both microtubule and actin filament inhibitors WE Theurkauf, TI Hazelrigg, personal communication.

The Exuperantia protein may mediate this microtubule-independent transport The cytoskeletal association of bicoid transcripts is stage specific During early oocyte accumulation, bicoid transcripts are associated with the cytoskeleton i. However, during stages 8—11, when bicoid transcripts are at the anterior margin of the oocyte, they are not cytoskeleton associated.

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This observation supports the idea that anchoring at the anterior pole at these stages is accomplished by some other structures. Later, during stage 14, bicoid RNA is localized in a tight cap at the anterior, is again associated with the microtubule-based cytoskeleton, and its localization is again sensitive to colchicine. In early embryos, bicoid RNA is no longer restricted to the cortex and is not associated with the cytoskeleton This localization coincides with the initiation of oskar and Pgc translocation from the anterior pole of the oocyte to its posterior.

Thus it is likely that oskar and Pgc switch from the use of minus-end-directed microtubule motors to the use of plus-end-directed ones in order to achieve transport to the posterior. In capuccino and spire mutants oskar RNA is not localized to the posterior during stages 8 and 9, but instead oskar RNA is uniformly distributed throughout the oocyte 24 , These mutants cause an early cytoplasmic streaming during stage 7 and 8 instead of 10B 52 , suggesting that premature assembly of microtubules into the parallel arrays in the subcortex drives cytoplasmic streaming In other words, oskar RNA does not localize to the posterior in capuccino and spire mutants because these mutants omit the stage during which antero-posterior axial organization of microtubules is used for directed transport of oskar RNA to the posterior.

Evidence suggests a role for the actin-based cytoskeleton at the anterior of the oocyte in transfer of RNAs to the microtubules that run from the anterior to the posterior pole.

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  • In oocytes that are mutant for a component of the actin-based cytoskeleton—cytoplasmic nonmuscle tropomyosin II cTmII — oskar RNA remains anteriorly localized at stage 9 and never localizes posteriorly , This observation suggests a role for cTmII—and possibly the actin-based cytoskeleton—in transfer of oskar RNA to the axial microtubules. Staufen protein similarly fails to translocate posteriorly in cTmII mutants , suggesting that the entire transport particle containing Staufen protein and oskar RNA fails to be transferred to the posterior translocation apparatus.

    As discussed above, the dynamics of transcript localization to the vegetal pole of Xenopus oocytes can largely be classified into two different patterns exemplified by Vg1 and Xcat-2 RNAs. This step appears to be mediated by selective entrapment of these RNAs, possibly similar to posterior polar-granule-localized RNAs in Drosophila see below. Xcat-2 RNA then relocates to form a disc-like pattern at the tip of the vegetal pole Vg1 RNA is initially generally distributed in the oocyte and later localizes in the wedge-shaped pattern that overlaps but differs from that of Xcat-2 RNA at the vegetal pole Accumulation of Vg1 to the vegetal pole requires functional microtubules but not actin microfilaments Later Vg1 RNA is found throughout the cortex of the vegetal hemisphere, unlike Xcat-2 , which is localized to a more restricted area at the vegetal pole During this late stage, Vg1 RNA is enriched to fold in the detergent-insoluble fraction Moreover, this association and cortical Vg1 RNA localization are not sensitive to microtubule-depolymerizing drugs nocodazole and colchicine but rather to microfilament-disrupting agents cytochalasin B This is an indication of a two-step localization mechanism for Vg1 RNA where microtubules are required for translocation and actin filaments for anchoring This localization is dependent on microtubules and cannot occur in late oocytes stage VI when microtubules are no longer present In addition, injected Xcat-2 transcripts that localize to the vegetal cortex without METRO do so in a pattern similar to Vg1 throughout the vegetal hemisphere but different from that of endogenous Xcat-2 transcripts Thus the differences in Vg1 and Xcat-2 localization patterns are a consequence of the fact that Xcat-2 is normally associated with the METRO, rather than in some inherent difference in their ability to associate with the microtubule-based cytoskeleton.

    Observations of localized RNAs in living neurons in culture have suggested that they are present in particles composed of several RNAs and proteins including polyribosomes These particles translocate inside the cell in a microtubule- but not microfilament-dependent manner Mammalian tau mRNA is localized to the proximal hillock of axons Moreover, this localization is dependent first on microtubules and then on actin microfilaments, as for Vg1 RNA This observation demonstrates that once an RNA associates with the cytoskeletal transport apparatus, it localizes according to the type of cell in which it is.

    This occurs even if that RNA normally would not be present in this cell type.

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    • Thus the role of the cytoskeleton in RNA localization is highly conserved across evolution see below. RNA localization also occurs in the yeast S. In this budding yeast, ASH1 mRNA is localized first to the future bud site and then to the daughter cell by a mechanism involving actin microfilaments , The role of microfilaments was demonstrated genetically using mutants in actin, myosin, profilin, and tropomyosin which form part of the microfilament network.

      In contrast, disruption of microtubules by tubulin mutants, or disruption of the process of budding with MYO2 mutants, has no effect on ASH1 transcript localization.

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      In various somatic cells e. This localization is not dependent on microtubules or intermediate filaments but on microfilaments Both RNA transport and anchoring are dependent on the actin cytoskeleton The data described above indicate a key role for microtubules in directed mRNA transport, especially in Drosophila and Xenopus oocytes but also in polarized cells such as neurons and glia.

      In several cases, microfilaments also play a crucial role in RNA localization.