nanos


DEVELOPMENTAL BIOLOGY

Nanos accumulation in the oocyte

Early in oogenesis (stages 4-5), NOS RNA synthesized in nurse cells accumulates in the oocyte, uniformly distributed until stage 9 when it accumulates in the oocyte's anterior margin. By stage 10, marking mid-oogenesis, the RNA becomes uniformly distributed again, and there is a high level of expression in nurse cells. This newly transcribed RNA is deposited in the oocyte following stage 10, and becomes posteriorly localized (Wang, 1994).

Embryonic

nos transcript is concentrated at the posterior pole in cleavage embryos and freshly laid eggs. At the pole bud stage (stage 3 early in zygotic development), the transcript segregates into the nascent pole cells. The transcript remains concentrated in the pole cells during blastoderm stages. During gastrulation and germ band extension, when the pole cells are carried dorsally and internalized into the embryo, staining for NOS mRNA is visible in the pole cells, but staining is not detected once pole cells have left the pocket formed by the posterior midgut invagination. After fertilization NOS protein is transcribed during the syncytial stage, emanating from the posterior pole and extending a short distance anteriorly (Lehmann, 1991 and Smith, 1992).

Translational repression of maternal Nanos (NOS) mRNA by a cis-acting Translational Control Element (TCE) in the NOS 3'UTR is critical for anterior-posterior patterning of the Drosophila embryo. It has been shown, through ectopic expression experiments, that the NOS TCE is capable of repressing gene expression at later stages of development in neuronal cells that regulate the molting cycle. These results predict additional targets of TCE-mediated repression within the nervous system. They also suggest that mechanisms that regulate maternal mRNAs, like TCE-mediated repression, may function more widely during development to spatially or temporally control gene expression (Clark, 2002).

To explore the possibility that other mRNAs may be regulated by the TCE or a TCE-like motif at different developmental stages, whether the TCE could repress translation in sites other than the Drosophila oocyte and early embryo was investigated. Evidence is provided that TCE-mediated repression can occur in a subset of cells in the central nervous system, by using the GAL4/UAS system to ectopically express either a regulatable NOS mRNA, which bears the TCE, or an unregulatable NOS mRNA, which lacks the TCE, in a variety of temporal and spatial patterns during development. Production of Nos from the unregulatable NOS mRNA in these cells produces a characteristic adult phenotype. Strikingly, this phenotype is suppressed when NOS RNA bearing the TCE is expressed in the identical cells. The phenotype caused by ectopic Nos resembles one caused by ablation of neurosecretory cells that produce eclosion hormone (EH). However, TCE-mediated regulation does not occur in EH cells themselves, but in other cells that act within this complex neuroendocrine signaling pathway. The ability of the TCE to repress Nos activity in the nervous system implies that TCE-mediated repression may be a more general mechanism for both spatial and temporal control during development (Clark, 2002).

Effects of Mutation or Deletion

Embryos derived from nanos mutant females lack all abdominal segments while the regions anterior (the head and thorax) and posterior (the telson) to the abdomen appear normal (Lehmann, 1988).

Anteroposterior polarity of the Drosophila embryo is initiated by the localized activities of the maternal genes, bicoid and nanos, which establish a gradient of the Hunchback (HB) morphogen. Nanos determines the distribution of the maternal HB protein by regulating its translation. To identify further components of this pathway, suppressors of nanos have been isolated. In the absence of nanos, high levels of HB protein repress the abdomen-specific genes knirps and giant. In suppressor-of-nanos mutants, knirps and giant are expressed in spite of high HB levels. The suppressors are alleles of Enhancer of zeste (E[z]) a member of the Polycomb group (Pc-G) of genes. E(z), and likely other Pc-G genes, are required for maintaining the expression domains of knirps and giant initiated by the maternal HB protein gradient. (Pelegri, 1994).

In a variety of tissues in eukaryotes, multipotential stem cells are responsible for maintaining a germinal population and generating a differentiated progeny. The Drosophila germline is one such tissue where a continuous supply of both eggs and sperm relies on the normal functioning of stem cells. Recent studies have implicated a possible role for the posterior determinant gene nanos (nos) in stem cells. nanos is required in the Drosophila female germline as well as in the male germline. In the female, nos is required for the functioning of stem cells. In nos mutants, while the stem cells are specified, these cells divide only a few times at the most and then degenerate. The loss of germline stem cells in nos mutant mothers appears to be due to a progressive degeneration of the plasma membrane. Furthermore, following germ cell loss, the germaria in the nos mutant mothers appear to carry on massive mitochondrial biogenesis activity. Thus, the syncytia of such germaria are filled with mitochondria. In the male germline, the male fertility assay indicates that nos appears to be also required for the maintenance of stem cells. In these mutant males, spermatogenesis is progressively affected and these males eventually become sterile. These results indicate novel requirements for nos in the Drosophila germline (Bhata, 1999).

To determine the ovarian phenotypes in nos mutant females, ovaries from nos mutant mothers were stained with Hoechst, a DNA stain, and then examined under a fluorescent microscope. In wild type, each ovariole contains six to seven developing egg chambers at different stages and generally one, but occasionally two, mature eggs. In nos mutant mothers, the ovaries contain ovarioles with either no egg chambers or a single to a maximum of seven egg chambers at different stages. Some of the ovarioles in nos mutants produce only one egg. In addition, the Hoechst staining of mutant ovaries indicates that ovaries with no developing germ cells can also be observed among nos mutant females. These results are consistent with the observation that ovarioles in nos ovaries produce a variable number of eggs and argue that the egg-laying defect in nos mothers is due to an interruption in the oogenesis process itself (Bhata, 1999).

Because the strong loss-of-function alleles of nos produce only a few eggs, it is possible that the germline stem cells are not specified in nos mutants and that the few eggs deposited by the mutant females are due to a subset of prestem cells that differentiate directly without going through a stem cell stage. Alternatively, one can also suppose that the loss of nos function affects the functioning but not the specification of stem cells and that the few eggs generated are due to both direct differentiation of prestem cells and to stem cells asymmetrically dividing a few times to produce a limited number of eggs. To distinguish between these two possibilities, first the egg-laying pattern of nos mutant females was determined. Because each asymmetric division of a stem cell yields one egg, determining the pattern and the number of eggs deposited over a period of time in a given mutation indicates the functional history of stem cells in that mutation. In wild type, a stem cell divides once in 12-22 hr to self-renew and to produce a cystoblast. A cystoblast undergoes 6-7 days of development before being deposited as an egg. A female Drosophila begins to lay eggs by its second day of emergence, indicating that parent cystoblasts for these eggs enter the differentiation pathway in the early pupal stage (the pupal stage extends for ~5 days at room temperature). Generally, a wild-type female deposits an average of 30-40 eggs per day for ~4 wk, after which the number becomes progressively reduced. nos females show three different types of disrupted egg-producing patterns. In Type I, nos females begin to deposit their eggs by the second day of emergence as in wild type, indicating that the process of egg development is not delayed in the mutants. However, these nos females stop laying eggs altogether by their fifth to ninth day of emergence. In Type II, nos mothers begin to deposit their eggs by their second day of emergence and cease egg laying between the fifth to ninth day, as in Type I; however, after an interval of 2 to 12 days of no egg deposition, these females lay a few more eggs. In Type III, nos mutant females do not lay any eggs. Phenotypic analysis of these mutant ovaries indicates that the ovarioles in Type III individuals are rudimentary and devoid of any developing egg chambers or other developing germ cells (Bhata, 1999).

The results presented in this article indicate that nos is required for the survival of stem cells in the female germline but not for their formation or specification. At least two different lines of evidence indicate that stem cells are indeed specified in nos mutant ovaries. First is the Type II egg-laying pattern displayed by nos mutant females; while the first batch of eggs in Type II may also contain eggs originating from a direct differentiation of prestem cell, the second peak of eggs (which are laid as late as 12 days after eclosion) are likely to have been generated from the asymmetric division of stem cells because all the prestem cells would have been differentiated and laid as eggs within the first 2-3 days of eclosion. Thus, the Type II egg-laying pattern indicates that stem cells are specified in nos mutant females and also that stem cells divide transiently to generate a few cystoblasts.

The second line of evidence comes from the staining pattern of the mutant germaria with several cell-type specific markers: in freshly eclosed females, the germaria in a large number of ovarioles in nos mutants appear to be wild type, with cells that would account for stem cells, cystoblasts, and two-cell cystocytes in region 1. In older females, however, only the stem cells can be observed at the tip of the germarium, not the cystoblasts or the cystocyte clusters. Additional indication that the large cells at the tip of the germarium are indeed stem cells is provided due to their lack of Bag of marbles mRNA, a cystoblast specific marker. In contrast, ovarioles of 4- to 5-day-old mutants containing only stem cells in the germarium and a few egg chambers in the vitellarium indicate that stem cells have divided earlier to generate a few cystoblasts. Moreover, the presence of empty agametic regions between stem cells and cystocyte clusters (as revealed by Orb staining) within the germarium of 2- to 3-day-old nos mutants argues that stem cells are, indeed, specified in nos mutants; however, they fail to generate cystoblasts in an uninterrupted manner (Bhata, 1999).

The requirements for the multi sex combs (mxc) gene during development have been examined to gain further insight into the mechanisms and developmental processes that depend on the important trans-regulators forming the Polycomb group (PcG) in Drosophila. Although mxc has not yet been cloned, it is known to be allelic with the tumor suppressor locus lethal (1) malignant blood neoplasm [l(1)mbn]. The mxc product is dramatically needed in most tissues because its loss leads to cell death after a few divisions. mxc also has a strong maternal effect. Hypomorphic mxc mutations are found to enhance other PcG gene mutant phenotypes and cause ectopic expression of homeotic genes, confirming that PcG products are cooperatively involved in repression of selector genes outside their normal expression domains. The mxc product is needed for imaginal head specification, through regulation of the ANT-C gene Deformed. This analysis reveals that mxc is involved in the maternal control of early zygotic gap gene expression known to involve some other PcG genes and suggests that the mechanism of this early PcG function could be different from the PcG-mediated regulation of homeotic selector genes later in development (Saget, 1998).

Induction of uncontrolled growth and deregulation of Hox genes are linked in mammals, where Hox products can induce leukemia. In Drosophila, modification of homeotic gene expression causes homeosis, sometimes associated with increased proliferation but not with uncontrolled tumorous growth, possibly because the identity of each segment is specified by a combination of HOM products. Loss or gain of one HOM gene will likely lead to a new combination that is found elsewhere in wild type, and cells expressing this combination could be expected to follow the corresponding developmental pathway and give rise to homeotic transformations. However, because each cellular identity apparently corresponds to a given proliferation rate, loss or ambiguity of identity due to deregulation of several selector genes in a single cell, such as mxc mutations apparently induce, could lead to loss of proliferation control. Identification of mxc partners and targets, as well as of the molecular nature of the mxc product, may help throw light on the genes and mechanisms involved in this process (Saget, 1998).

It has been proposed that certain PcG genes are required for the maintenance of the expression domains of knirps and giant, through a mechanism similar to the regulation of homeotic genes. The regionalization of the Drosophila embryo depends on the maternally supplied products of bicoid (bcd), hunchback (hb), and nanos (nos). Nos represses the translation of the maternal HB mRNA in the posterior embryonic region. This permits the expression of the zygotic gap genes knirps (kni) and giant (gt), which specify posterior identities. These genes would otherwise be repressed by Hb. Embryos from nos/nos mothers form no abdominal segments, but this phenotype can be rescued by a total lack of hb in the maternal germline. It can also be dominantly rescued by the mutation of maternally supplied regulator molecules that normally repress kni and gt in the zygote. Pelegri and Lehmann (1994) have shown that certain mutant products of the PcG genes E(z), Psc, and pleiohomeotic can partially rescue nos by such a maternal effect. To determine if mutation of mxc also affects this regulation, the cuticles of embryos were examined from mxc/+;hb nos/nos mothers that were heterozygous for different mxc mutations. This genetic background was used because a decrease in the amount of maternal hb product can partially rescue the nos phenotype in F1 embryos. Such embryos can differentiate a few abdominal denticle belts and form an adequate background to evaluate increased rescue of nos. Thus loss-of-function PcG mutations should have a strong effect on rescue, and the embryos from hb nos/nos mothers that have two PcG mutations in their genetic background should permit increased rescue of the nos phenotype (Saget, 1998).

Any of three E(z)son (suppressor of nanos) alleles or a hypomorphic pleiohomeotic allele partially rescue the phenotypes of hb nos/nos progeny by a maternal effect; deficiencies covering E(z) or the Psc/Su(z)2 complex also allow some maternal rescue of hb nos/nos progeny, yet the strongest effect is observed with the gain-of-function E(z)son alleles. The EMS-induced allele mxcG48 rescues the hb nos/nos progeny phenotype, whereas a deficiency of mxc does not. Some rescue with the Psc/Su(z)2 complex deletion Df(2)vgB is also observed and strong rescue (consistently >50%) is observed with an EMS-induced pleiohomeotic allele phob, described as amorphic. This suggests that phob and mxcG48 are probably not amorphic alleles, and that maternal rescue of hb nos/nos progeny by a PcG gene is most efficient with a non-null mutation (Saget, 1998).

Segmentation of embryos from transheterozygous mothers was also examined. Because neither a reduction of wild-type PcG product nor two PcG mutations in trans in the hb nos/nos mothers increases nos rescue, these data strongly suggest that, whatever the mechanism of gap gene regulation by these PcG mutations may be, it does not function like the PcG-mediated maintenance of homeotic gene expression in embryos and in imaginal discs. The strong rescue provided by several non-null EMS-induced mutations, which may produce mutant proteins, leads to a proposal that modified PcG proteins are poisoning a normal process. How this process depends on wild-type regulation by PcG products has yet to be established (Saget, 1998).

The zinc-finger protein Nanos functions during development (to promote germ cell migration) and during oogenesis (during germ line stem cell development). In a third role, early in development, Nanos and the RNA-binding protein Pumilio act together to repress the translation of maternal hunchback RNA in the posterior of the Drosophila embryo, thereby allowing abdomen formation. Nanos RNA is localized to the posterior pole during oogenesis; the posteriorly synthesized Nanos protein is sequestered into the germ cells as they form in the embryo. This maternally provided Nanos protein is present in germ cells throughout embryogenesis. Maternally deposited Nanos protein is essential for germ cell migration.

In embryos lacking maternal Nos, defects in germ cell migration are seen from stage 10 onward. Following the exit of germ cells from the posterior midgut pocket, the germ cells fail to migrate over the surface of the gut and instead cluster tightly together on the outer gut surface. In many embryos most of the germ cells remain in a large cluster associated with the distal tip of the posterior midgut as it extends anteriorly during embryonic development. Mutant germ cells seem to cluster very tightly together as soon as they exit the midgut whereas, in wild type embryos, this tight association between germ cells is only seen following their association with the gonadal mesoderm at a later stage in embryogenesis. Zygotic nos expression cannot compensate for the loss of maternal Nos (Forbes, 1998).

Lack of zygotic nanos and pumilio activity in adults has a dramatic effect on germline development of homozygous females. Given the coordinate function of nanos and pumilio in embryonic patterning early in development, an analysis was made of the roles of these genes in oogenesis. Both genes act in the germline. Although the nanos and pumilio ovarian phenotypes have similarities and both genes ultimately affect germline stem cell development, the focus of these phenotypes appears to be different. While pumilio mutant ovaries fail to maintain stem cells and all germline cells differentiate into egg chambers, the focus of nanos function seems to lie in the differentiation of the stem cell progeny, the cystoblast. Thus, in egg chambers pum acts early in the developmental hierarchy in the maintenance of stem cells and nos functions later in stem cell progeny (Forbes, 1998).

When comparing pum and nos mutant germaria, and consistent with differences in their effects on early oogenesis, differences in the distribution of Spectrin are also seen. In nos mutants, very small spectrosomes are seen in the germline stem cells closely associated with the cell membrane adjacent to the cap cells. The amount of Spectrin associated with the fusome in the dividing germline cysts is greatly reduced in nos mutants. This phenotype suggests that while stem cells are established in nos mutants, they are not entirely normal. In pum mutant germaria, Spectrin-staining dots, which are almost as large as in wild type but more irregularly shaped, are seen in the most anterior germline cells. However, in contrast to wild-type stem cells, these spectrosome-containing cells are not associated with the basal cells of terminal filaments or cap cells. This is consistent with the failure to maintain germline stem cells at the germarium tip in pum mutants. Consistent with the model that nanos and pumilio have different phenotypic foci during oogenesis, high levels of Pumilio protein are detected in the germline stem cells and high levels of Nanos in the dividing cystoblasts. Therefore, it is suggested that in contrast to early embryonic patterning, Nanos and Pumilio may interact with different partners in the germline (Forbes, 1998).

The maternal RNA-binding proteins Pumilio (Pum) and Nanos (Nos) act together to specify the abdomen in Drosophila embryos. Both proteins later accumulate in pole cells, the germline progenitors. Nos is required for pole cells to differentiate into functional germline. Pum is also essential for germline development in embryos. A mutation in pum causes a defect in pole-cell migration into the gonads. In such pole cells, the expression of a germline-specific marker (PZ198) is initiated prematurely. pum mutation causes premature mitosis in the migrating pole cells. Pum is found to inhibit pole-cell division by repressing translation of cyclin B messenger RNA. Since these phenotypes are indistinguishable from those produced by nos mutation, it is concluded that Pum acts together with Nos to regulate these germline-specific events (Asaoka-Taguchi, 1999).

The Drosophila protein Nanos encodes an evolutionarily conserved protein with two zinc finger motifs. In the embryo, Nanos protein function is required for establishment of the anterior-posterior body pattern and for the migration of primordial germ cells. During oogenesis, Nanos protein is involved in the establishment and maintenance of germ-line stem cells and the differentiation of oocyte precursor cells. To establish proper embryonic patterning, Nanos acts as a translational regulator of Hunchback RNA. Nanos' targets for germ cell migration and development are not known. A selective genetic screen was carried out aimed at isolating new nanos alleles. The molecular and genetic analysis of 68 new alleles has allowed the identification of amino acids critical for nanos function. This analysis shows that the CCHC motifs, which coordinate two metal ions, are essential for all known functions of Nanos protein. Furthermore, a region C-terminal to the zinc fingers seems to constitute a novel functional domain within the Nanos protein. This 'tail region' of Nanos is required for abdomen formation and germ cell migration, but not for oogenesis (Arrizabalaga, 1999).

The last 87 amino acids of Nanos contain two metal-binding domains of the CCHC type. In addition to mutations that alter the CCHC motif and thereby affect the ability of the mutant protein to chelate Zn, mutations in 9 amino acids located within the Zn finger domain that completely abolish nanos function were identified. While these mutations could affect the structure or stability of the protein, some of these mutations may identify amino acids important for the ability of Nanos protein to interact with RNA or protein targets. Zinc fingers of the CCHC type are not commonly found. The spacing between the Cys and His residues in Nanos are unique to this protein and its homologs. Other proteins, such as the HIV nucleocapsid protein, Xenopus CNBP, and Drosophila Clipper, have multiple copies of CCHC zinc fingers, but the ligand spacing is different. All of these proteins have been implicated in binding to single-stranded RNA. For instance, Clipper (Clp) is a Drosophila endoribonuclease that cleaves RNA hairpins. This protein contains five CCCH fingers that confer the endonucleolytic function and two CCHC fingers implicated in specific RNA binding. In addition to the CCHC motif, the HIV-I nucleocapsid protein and Nanos share a seven-amino-acid spacing between the zinc fingers. Of particular interest is the fact that the fourth amino acid in this spacer is an Arg in both proteins. The mutational analysis has identified this Arg351 as important for nanos function. This Arg is conserved among HIV nucleocapsid proteins and has been shown to be required for viral genomic packaging. In addition, crystallography studies of the nucleocapsid protein bound to its RNA target shows that this Arg makes direct contact with nucleic acids. Thus, it is an intriguing possibility that this Arg plays a similar role in Nanos (Arrizabalaga, 1999 and references therein).

The specific function of the zinc fingers in Nanos is not known. However, it has been shown that Nanos can bind to RNA with high affinity and that the ability of Nanos to bind RNA resides in the C terminus. While a specific, high-affinity interaction between Nanos and the NREs has not been established, Pumilio protein has been shown to bind with high affinity and specificity to the NREs. Point mutations in the NREs that affect Pumilio binding do not affect the affinity of Nanos for the RNA. Nevertheless, a small number of nucleotides outside the conserved NRE motif have been shown to affect translational regulation of hunchback binding, but not Pumilio binding. Further experiments are required to determine whether Nanos indeed binds to the NREs or other RNA targets with sequence specificity and whether Arg351 plays a role in such an interaction (Arrizabalaga, 1999 and references therein).

Mutations in a region C terminal to the zinc fingers of Nanos cause abdominal and germ cell migration defects without affecting the function of nanos in oogenesis. Since increasing the dosage of Nanos protein containing a mutation in the tail domain does not alter the abdominal phenotype of mutant embryos, the hypothesis is favored that the tail region of Nanos constitutes a separate functional domain. Mutations in the tail domain affect germ cell migration differently from nanos null mutations. Null mutations or mutations in the zinc finger region of Nanos have been shown to have a dramatic effect on germ cell migration. Primordial germ cells devoid of Nanos have altered morphology, fail to leave the gut toward the mesoderm, and tightly associate with each other in clusters. Furthermore, enhancer trap lines that are normally expressed in germ cells late during embryogenesis are expressed earlier in nanos mutant germ cells. This has led to the hypothesis that some of the phenotypes displayed by nanos mutant germ cells may be caused by the precocious expression of genes normally expressed at a later stage. Mutants in the tail domain affect germ cell migration to a lesser extent than null mutations. nosL7 germ cells, like germ cells lacking Nanos, form clusters and fail to leave the gut. However, aberrant germ cell clustering is not as extreme as that seen for the null mutant, and germ cell morphology seems normal. Furthermore, premature gene expression has not been observed in nosL7 mutants. Finally, many nosL7 germ cells reach the embryonic gonad and the embryos develop into fertile adults (Arrizabalaga, 1999 and references therein).

These differences in phenotypes might indicate that nosL7 is a weak allele with respect to germ cell migration. Contrary to what is observed in hunchback regulation, nosL7 may retain some function in germ cell migration. Alternatively, the tail domain may just affect a subset of the processes disrupted in the null mutants. Contrary to nosL7 germ cells, nanos null germ cells show aberrant morphology and even when some cells reach the gonad, the resulting adults are often sterile. Consequently, nanos might be required in the germ cells for two independent functions: migration, which requires the tail domain, and germ-line stem cell identity, which does not require the tail domain. Problems in germ cell identity might exacerbate the migration defect, hence the greater loss of germ cells in the null mutants. Clearly, the identification of Nanos germ-line targets is required to further address the function of its different domains in germ cell migration (Arrizabalaga, 1999).

The Nanos CCHC motifs show significant homology with sequences from other insects, Xenopus, leech, and C. elegans. The Xenopus nanos homolog Xcat-2 and the leech homolog are expressed in the developing oocyte. Xcat-2 RNA is localized to the vegetal pole of the oocyte during oogenesis. In the embryo, Xcat-2 RNA is initially taken up into the vegetal blastomeres and its expression becomes restricted to the primordial germ cells later in embryogenesis. The function of the Nanos homolog in Xenopus is not known. However, the similarity in localization pattern suggests a role for the protein in establishing embryonic polarity or germ-line development. Most amino acids mutated in this screen are conserved in these divergent species. Only two mutations, alleles nos538/549 and nos512, lead to changes in nonconserved amino acids (V354M and S337L). Given that these amino acids are next to His and Cys residues of the CCHC motif, it is possible that these mutations may affect the metal coordination within their respective zinc fingers. Despite the high degree of conservation between the two zinc finger domains of Drosophila Nanos and Xenopus Xcat-2, the two protein regions are functionally not interchangeable. . An RNA in which the Nanos zinc fingers were replaced in frame by those of Xcat-2 was shown to be unable to rescue the nanos mutant abdominal phenotype (Arrizabalaga, 1999 and references therein).

Three family members of Nanos have been identified in C. elegans, and a role for these three proteins in germ-line development has been suggested. Among the three C. elegans Nanos homologs, the characteristic CCHC motif with the exact spacing within and between the two fingers is only conserved in Nos-3. Like Xcat-2, the homology between Drosophila Nanos and the C. elegans homolog includes only the zinc finger region, while there is no homology with the tail domain. The results presented in this paper suggest that the tail domain of Nanos is specifically required for the regulation of hunchback and bicoid and certain aspects of germ cell migration. One explanation for the functions of the tail domain and the zinc finger is that the tail domain carries out functions that are unique to insect development, while the zinc finger domain plays a conserved role in germ-line development. In support of a conserved role for Nanos, homologs of Pumilio, the functional partner of Nanos, have been found in many species, including C. elegans. There are at least eight pumilio homologs in C. elegans, and the role of two functionally redundant homologs, FBF1 and FBF2, has been reported. Fem-3 binding factor (FBF) proteins, like their Drosophila counterpart, are specific RNA-binding proteins and act as translational repressors. One of the identified FBF targets is the fem-3 gene, which is involved in germ-line sex determination. Fem-3 directs spermatogenesis in the hermaphrodite, and its translation must be suppressed to allow the switch to oogenesis to occur. These observations suggest a role for FBF in translational regulation similar to that performed by Pumilio and Nanos in Drosophila. Furthermore, the fact that the FBFs like Pumilio and Nanos regulate germ-line cell fate may suggest a conserved role for Nanos and Pumilio in germ-line development (Arrizabalaga, 1999 and references therein).

In summary, the analysis of a large number of nanos mutants has led to the following model for Nanos protein function: the C terminus of Nanos plays a crucial role during three developmental stages of Drosophila development: embryogenesis, primordial germ cell migration, and oogenesis. Nanos' role during embryogenesis is to silence the translation of maternal Hunchback RNA. This function requires the Nanos zinc finger and tail region as well as the RNA-binding protein Pumilio. During primordial germ cell development, Pumilio and Nanos are required for migratory behavior, the temporal control of gene expression, and the differentiation of germ cells into germ-line stem cells. These processes require Pumilio and the zinc finger region of Nanos. The function of Nanos' tail region seems to be restricted to certain aspects of germ cell migration. During oogenesis, only the zinc finger region is necessary for Nanos' function, which has aspects both overlapping with and separate from Pumilio. Nanos homologs in other organisms suggest a conserved role in germ cell development. In these organisms, the region of homology is restricted to the zinc finger motif and does not span the tail domain, suggesting that the tail domain may have been recruited later in evolution and may fulfill a more specialized roles (Arrizabalaga, 1999).

nanos is required for formation of the spectrosome, a germ cell-specific organelle

Germ cell identity and development are controlled by autonomous cues in the germ plasm as well as by interactions between germ cells and somatic cells. This study investigated the formation of a germ cell-specific organelle, the spectrosome. Spectrosome formation is independent of germ cell-soma interactions and is autonomous to the germ cells. Furthermore, the germ plasm component nanos (nos) is essential for spectrosome formation. The role of nos in spectrosome formation is independent of its role in germ cell survival; nos mutant germ cells that are prevented from undergoing programmed cell death still fail to form spectrosomes. Thus, nos is required to regulate the formation of this germ cell-specific organelle, further supporting a role for nos in promoting germ cell identity (Wawersik, 2005).

nanos and pumilio are essential for dendrite morphogenesis in Drosophila peripheral neurons

Much attention has focused on dendritic translational regulation of neuronal signaling and plasticity. For example, long-term memory in adult Drosophila requires Pumilio (Pum), an RNA binding protein that interacts with the RNA binding protein Nanos (Nos) to form a localized translation repression complex essential for anterior-posterior body patterning in early embryogenesis. Whether dendrite morphogenesis requires similar translational regulation has been unknown. nos and pum are shown in this study to control the elaboration of high-order dendritic branches of class III and IV, but not class I and II, dendritic arborization (da) neurons. Analogous to their function in body patterning, nos and pum require each other to control dendrite morphogenesis, a process likely to involve translational regulation of nos itself. The control of dendrite morphogenesis by Nos/Pum, however, does not require hunchback, which is essential for body patterning. Interestingly, Nos protein is localized to RNA granules in the dendrites of da neurons, raising the possibility that the Nos/Pum translation repression complex operates in dendrites. This work serves as an entry point for future studies of dendritic translational control of dendrite morphogenesis (Ye, 2004).

Early in Drosophila embryogenesis, Nos protein is first detected in the posterior end of the embryo and then in the pole cells, whereas Pum protein is uniformly distributed. Characterization of later expression has been limited to the ovary for Nos and to the adult head for Pum. Several recent findings implicate Nos and Pum in eye development, optic nerve development, neuronal excitability, and long-term memory. To determine whether Nos and Pum regulate dendrite morphogenesis, their expression and function were examined in the dendritic arborization neurons in the Drosophila peripheral nervous system (PNS) (Ye, 2004).

The da neurons have proven to be useful for studies of dendrite development. The 15 da neurons in each hemisegment of larvae fall into four classes (class I, II, III, and IV) with increasing complexity of dendritic morphology. The highest order dendrites of class I and II da neurons are fourth-order dendrites. Most of the terminal branches of class III neurons are fifth-order dendrites with a distinctive structure referred to as dendritic spikes. The class IV neurons have highly branched dendrites with terminal branches typically above the fifth-order (Ye, 2004 and references therein).

Nos and Pum were expressed in all da neurons, as revealed by immunocytochemistry with antibodies against Nos or Pum in third-instar larvae from a transgenic line carrying GFP marker 80G2, which marks all da neurons. Neuronal expression of nos was further confirmed with two independent GAL4 drivers under the control of the nos promoter, P{GAL4-nos.NGT}40. mCD8-GFP immunoreactivity is observed in da neurons of larvae that carry both P{GAL4-nos.NGT}40 and a reporter gene, UAS-mCD8-GFP, suggesting that the nos promoter is active in da neurons. Similar neuron-specific expression was also observed with nos-GAL4::VP16, which was inserted into a different chromosome and yielded some segment-to-segment variations in the expression pattern (Ye, 2004).

Overexpression of nos-tub3′UTR in class III and class IV neurons, but not class I neurons, dramatically changes dendrite morphology. In both class III and class IV neurons, the number of high-order dendritic branches was significantly reduced while the morphology of the major branches was not affected. Overexpressing pum causes a similar change specific to dendrites of class III and IV neurons. Neither the dendrites of bipolar neurons nor those of chordotonal neurons were affected by overexpressing nos or pum (Ye, 2004).

The loss of function phenotype of nos and pum in dendrite morphogenesis was assessed via mosaic analysis with a repressible cell marker (MARCM). The MARCM system provides an effective way to study every type of PNS neuron, including da neurons, chordotonal neurons, bipolar neurons, and external sensory (es) neurons, with single cell resolution. It was therefore determined which of these neurons is affected by nos or pum mutation. In addition, by specifically eliminating nos or pum function in da neurons, whether these genes act cell-autonomously in dendritic morphogenesis was determined. As a control, MARCM analysis was performed with a chromosome carrying an unrelated transgene (Ye, 2004).

Loss of nos or pum in class I or II da neurons did not alter dendrite morphology. In contrast, in class III neurons lacking nos or pum function, the characteristic dendritic spikes are significantly elongated, but the order of dendrites and the length of major dendritic branches (all dendrites except dendritic spikes) are indistinguishable from those of wild-type neurons. Whereas around 2%-10% of dendritic spikes of wild-type ddaA neurons are longer than 10 μm, loss of nos or pum function causes about 10%-30% of spikes to be longer than 10 μm in about 50% of ddaA neurons (Ye, 2004).

Class IV neurons deficient for nos or pum function also exhibit abnormality in their dendrites. The dendrites of wild-type class IV neurons cover the epidermis in a complete but nonoverlapping fashion and thereby 'tile' the body wall. Incomplete coverage of the epidermis was observed in 20% of neurons mutant for nos (3 in 15) as a result of the reduction of higher-order branches. Therefore, both nos and pum are required for the proper morphogenesis of dendrites, especially the high-order dendritic branches, in a cell type-specific manner (Ye, 2004).

Given the similar dendrite phenotypes of nos and pum mutants, it was wondered whether there is a mutual requirement of nos and pum for dendrite morphogenesis, as in embryogenesis. First it was tested whether pum function is required for nos overexpression to eliminate high-order dendritic branches in class IV neurons. Indeed, when nos is overexpressed in a pum null background, the high-order dendritic branches are not as drastically reduced as those in the case of nos overexpression in a wild-type background. It was then reasoned that, if nos and pum require each other in regulating dendrite morphogenesis, the dendrite phenotypes of pum, nos double mutants should resemble those of single mutants of nos or pum. MARCM analysis was employed to examine the dendrites of da neurons mutant for both nos and pum. Eliminating both nos and pum functions in class I da neurons does not result in any defect in dendrite morphology. The number of long dendritic spikes in class III neurons is increased to a similar extent as in the nos and pum single mutants. Moreover, incomplete innervation of the territory was observed in 18% of neurons mutant for both nos and pum (5 in 28 clones), an extent similar to that in the single mutant of either nos (20%) or pum (15%), as a result of reduced numbers of high-order branches in class IV neurons. Taken together, these data indicate that nos and pum require each other to regulate dendrite morphology, possibly by forming a protein complex as they do in embryogenesis (Ye, 2004).

The only domain structure identified so far in Pum protein is the so-called 'Pumilio-homology domain' (Pum-HD), which consists of eight repeats of 36 amino acids and is conserved in various species, including humans. Pum-HD is responsible for binding to the nos response elements (NRE's) of hb mRNA, and is sufficient for Pum function in embryogenesis. To investigate whether this RNA binding domain is sufficient for dendrite morphogenesis, Pum-HD was overexpressed in class IV da neurons. Overexpression of Pum-HD virtually replicates the dendrite phenotype that was produced by overexpression of full-length Pum. Therefore, it is likely that the Nos/Pum complex regulates the downstream molecules through the RNA binding domain of Pum (Ye, 2004).

If the roles of Nos and Pum in dendrite morphogenesis are to be fully understood, it is crucial to identify the RNA targets of this complex in dendrites. The dendrite phenotypes described here provide a guide for searching for the RNA targets of the Nos/Pum complex in an ongoing genetic screen for dendrite development. Moreover, the epitope-tagged Pum RNA binding domain, which is sufficient for Pum function in dendrites, will be a useful tool for biochemically identifying the RNA targets (Ye, 2004).

To elucidate the possible site of Nos/Pum action, the subcellular distribution of Nos was studied. Because the anti-Nos antibody also stains muscle in larvae, it was difficult to examine Nos distribution in neuronal processes situated near muscle. To circumvent this technical problem, a transgene of Nos fused to an HA-epitope tag at the N terminus was generated and it was expressed in da neurons, but not muscles, by using the GAL4/UAS binary system. HA-Nos is localized to distinctively punctuate structures in both soma and dendrites. These structures are round and uniform in size, with a diameter of around 0.3 μm; this is reminiscent of the RNA granules ranging from 0.175-0.6 μm in diameter in mammalian cortical neurons. Then the larval preparations were double stained with both anti-HA antibody and Syto 14, a nucleic acid dye that preferentially labels RNA; Nos was found to colocalize with RNA granules (Ye, 2004).

Essential for the posteriorly localized translation repression of hb by Nos/Pum complex, translation of Nos itself is repressed in the anterior of the embryo via a 90 nucleotide translational control element (TCE) located in the 3' untranslated region (3'UTR) of nos mRNA. In a subset of Drosophila central neurons, ectopic expression of nos causes the wing expansion phenotype only upon replacement of the TCE-bearing 3'UTR with α-tubulin (tub) 3'UTR (nos-tub3'UTR), thereby removing the TCE-dependent translational suppression of the nos transgene. To examine whether a mechanism analogous to that for the translational repression of nos in the embryo exists in da neurons, a GAL4 driver (GAL48-123) was used to ectopically express nos-tub3'UTR mRNA inserted with the nos TCE (nos-tub:nos+2). The nos-tub3'UTR and nos-tub:nos+2 transgenes have been shown to have little position effect in expression. Overexpression of nos-tub3'UTR resulted in reduction of the amount of high-order dendritic branches, a dendrite phenotype similar to that produced by GAL44-77. Overexpression of nos-tub:nos+2 with GAL48-123 significantly reduces the severity of the phenotype, thereby suggesting the presence of a mechanism for translational repression of nos in class IV da neurons (Ye, 2004).

Both nos and pum genes are conserved in various species, including mammals. Two nos genes have been identified in humans. The zygotic nos1 is highly expressed in the nervous system but not in developing germ cells. It is unclear whether nos2 and 3 are expressed in the nervous system. There have been no gross anatomical defects observed in mice deficient for nos1. In light of this study, it would be of interest to conduct a detailed investigation on neuron morphology with single-cell resolution to ascertain whether these mice exhibit any defects in dendrite morphology, especially of high-order dendritic branches. It is also important to determine whether nos2 and nos3 are expressed in the nervous system and if their functions are redundant to those of nos1. Two pum genes, pum1 and pum2, have been cloned in both mice and humans; both genes are expressed in the brain. It will be interesting to see whether these genes take on separate or redundant roles in neurodevelopment and long-term memory, both functions of the pum gene in Drosophila (Ye, 2004).

In summary, nos and pum have been shown to be essential for proper dendrite morphogenesis in subsets of Drosophila PNS neurons: evidence is provided suggesting that they act by forming a translation control complex, possibly in dendrites. This study could serve as a starting point for future identification and characterization of molecules regulating local translation in both Drosophila and mammalian dendrites (Ye, 2004).


nanos: Biological Overview | Evolutionary Homologs | Regulation | mRNA localization and post-transcriptional regulation | Developmental Biology | References

Home page: The Interactive Fly © 1997 Thomas B. Brody, Ph.D.

The Interactive Fly resides on the
Society for Developmental Biology's Web server.