Current Topics in Developmental Biology, Vol. 33

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However, usp and EcR mutants have somewhat different embryonic phenotypes, suggesting that EcR has additional functions that do not depend on usp [ ]. Nonetheless, as is the case for EcR, usp function is required in multiple tissues for cell survival and differentiation, consistent with its role as the cofactor for a global integrated hormonal response.

As described above, C. The retinoid-binding RXR receptors were first identified in on the basis of molecular properties in vertebrates [ , , ].

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Surviving animals are mostly normal, but males suffer from defects in spermatogenesis due to abnormalities in Sertoli cells [ ]. Studies have also identified roles for RXR receptors in cyclic metabolic functions in the liver and vasculature [ , ], suggesting some conservation of global temporal regulation reminiscent to usp function in the fly. Nonetheless, despite the apparent conservation of heterodimerization properties, this subfamily also demonstrates significant functional elaboration across animal phyla. The Drosophila HR78 gene was identified by molecular approaches as a nuclear receptor expressed during the onset of metamorphosis [ 19 ].

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Loss of HR78 results in arrest as undersized third instar larvae that fail to execute ecdysteroid-triggered events and have tracheal defects [ ]. HR78 coordinates with the SAM domain co-repressor Moses to help regulate cell proliferation, with HR78 activity favoring and Moses activity inhibiting cell division [ ]. Like HR78 , nhr is broadly expressed and oscillates with the molting cycle.

Knockdown of nhr results in SDS-sensitive dauer larvae, suggesting a defect in the dauer cuticle [ 25 ]. A probable null deletion of nhr is viable, suggesting that nhr plays a modest or partially-redundant developmental function in C. The TR2 gene NR2C1 of vertebrates was the founding member of this gene class, discovered by low-stringency hybridization from a human testis cDNA library [ ]. Deletion of TR2 does not result in testicular or spermatogenesis defects—homozygous null mutant mice are viable and fertile [ ].

A recent analysis has demonstrated that it regulates early transcription factors that coordinate the development of retinal progenitor cells and knockout mice have severe vision deficits [ ]. In contrast, knockout of the TR4 paralog NR2C2 has dramatic effects on mouse viability, with homozygotes dying either during fetal development or postnatally, with significant compromises in growth and reproductive behavior [ ].

Mutant mice also display severe motor deficits associated with aberrant cerebellar development, establishing a major role for TR4 in neuronal development [ ]. TR2 and TR4 appear to play partially-redundant functions in stem cell proliferation. Mice with both genes knocked out die during embryogenesis with increased apoptosis [ ]. Because of their potential as targets for anti-cancer therapies, interest in TR2 and TR4 remains high [ ].

In both flies and vertebrates, family members regulate cell proliferation events and play critical roles in development. In both flies and nematodes, they have regulatory patterns and functions associated with the molting cycle. However, the function in regulation of cell proliferation does not seem to have been maintained in C.

Deficiency in tll results in a failure to develop posterior body segments as well as parts of the brain, thus resulting in embryonic lethality. Loss of function in tll decreases neuroblast formation in the protocerebrum and no boundary is formed between the protocerebrum and the deutocerebrum [ , ]. The tll gene also plays a role in eye development, in both the eye-precursor cells and the embryonic optic lobe [ ].

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These important roles in neural identity and boundary formation appear to be well-conserved in other animals. Loss of tll in the adult fly pars intercerebralis leads to a loss of neuropeptide expression and increased aggression, although the specific developmental effect in this part of the brain has not been described [ ]. Identified by the C.

RNAi knockdown of nhr demonstrated a function in cuticle shedding, egg-laying and vulval development [ 25 ]. During the L2 and L3 stages, nhr functions in the differentiation of pre-VU and anchor cells of the ventral uterus [ ]. Defective anchor cells fail to invade the underlying vulval tissue and remain in the cell cycle, generating additional cells [ ]. Later in larval development, it plays a role in vulval morphogenesis [ ] and in the male it regulates the timing of the migration of the linker cell, which is the male equivalent of the anchor cell [ ].

Loss of nhr results in embryonic and L1 lethality [ ]. In the embryo, nhr is expressed in the posterior-most daughters of multiple lineages—reminiscent of the function of tll in Drosophila embryonic termini—and appears to be responsive to Wnt regulation [ ]. Tlx is expressed in the developing central nervous system—the telencephalon, diencephalon, eye and nasal placode [ , ]. Unlike its Drosophila and C.

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Mutant mice display varying levels of anatomical and behavioral abnormalities, including patterning defects in the brain, particularly at the pallio-subpallio boundary [ ]. Due to the limbic system's development from these early structures, adult knockout mice show significant behavioral changes, most notably high levels of aggression and poor maternal instincts [ ]. This may reflect a conserved function, since the fly pars intercerebralis is thought to be analogous to the vertebrate hypothalamus, and the same cofactor, Atrophin, participates in aggression in both flies and mice [ , ].

A variety of retinopathies also result from Tlx mutation, indicating that it plays a critical role in the development and maintenance of retinal cells [ ]. Tlx plays a role in neural stem cell self-renewal and adult neurogenesis [ ], where it functions upstream of a Wnt signaling pathway [ ]. In mutant Tlx mice, neural stem cells undergo precocious maturation to neurons and are therefore quickly depleted, resulting in mice with smaller gyrus and forebrain regions [ , ].

This premature cell cycle exit phenotype appears opposite to the cell cycle phenotype in the C. In summary, functions in neuron development, optic development, and cell cycle control appear to be conserved among NR2E1 gene family members. The unfulfilled HR51 gene was named on the basis of the mutant phenotype in which eclosed adults fail to unfold their wings and exhibit reduced fertility [ , ].

In mushroom bodies, it functions in specifying neuron identities and regulating axon pathfinding [ ]. More recently, unf has been implicated in circadian rhythms in Drosophila by functioning in the identity of small ventral Lateral Neurons as the master pacemaker [ ]. In late stage pupae, unf accumulates in the Mushroom Body of the brain and in some lateral neurons near the optic lobes. Mutations in fax-1 cause loss of expression of neuropeptides, neurotransmitter receptors, and other markers of interneuron identity [ , ]. Similar to the defective axon regrowth phenotype noted in unf mutants, fax-1 mutants display reduced axon regeneration of an interneuron following laser damage [ ].

Thus a conserved function in specifying neuronal identity and axonal growth appears to be a feature of this gene. PNR is an extreme example of a spatially restricted nuclear receptor, being expressed exclusively in the retina and pineal gland. In rod photoreceptors, PNR plays an important role in cell fate by repressing cone-specific genes [ , ]. Further, deletions in PNR in mice result in retinal degeneration consistent with flecked retinal degeneration in humans [ ]. PNR has been shown to interact with Rev-Erb, probably as a heterodimer [ ].

Mutations in human PNR result in inherited retinal degeneration diseases [ ].


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NR2E3 family members all seem to play roles in neuronal differentiation—and the common function in axonal arborization points to some more specific conservation of function between Drosophila and C. The function in photoreceptor development in vertebrates appears to be another example of exaptation, although in this case perhaps applying a conserved function in neuron differentiation to a new neuron type. There exist two additional gene classes in the NR2E family, but both appear to have been lost from vertebrates. Homozygous dsf females show resistance to copulation and fail to lay eggs when they do mate [ ].

These phenotypes may be explained by the lack of synapses present in the circumferential muscles of the uterus in mutant dsf females.

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Males also display striking courtship behavior phenotypes, including increased male-male courting, delayed copulation, and defects in abdominal curling during the final stage of courtship. These phenotypes may be explained by the irregular innervation of the ventral longitudinal muscles of abdominal segment 5, particularly the presence of a few large, spherical boutons on each fiber.

Thus dsf plays important roles in nervous system development. Once thought to be an arthropod innovation, dsf orthologs are now apparent in the genomes of lophotrochozoans and echinoderms. There is considerable divergence in the LBD of the nhr clade, and some species-specific orthologs have truncated LBDs. Mutations in HR83 are homozygous viable in the fly, but expression and function have not yet been described.

The NR2F class of nuclear receptors is well conserved and has been extensively studied. Drosophila seven-up svp functions in a diverse set of cell specification and transcriptional regulation roles.


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Loss of svp results in transformation of R1, R3, R4, and R6 photoreceptors of the compound eye into R7 photoreceptors. Over expression results in a loss of R7 and R8, indicating that it plays a sufficient role in sensory neuron specification [ ]. The gene is also required for specification and development of fat body cells [ ], cell proliferation in Malpighian tubule development [ ], and proper cardioblast diversification by repressing tinman in a subset of cells [ ].

The VD motor neurons of unc mutants are transformed to resemble the afferent and efferent synaptic patterning of DD motor neurons. Therefore, unc functions in specifying neuronal identities, similar to the role of its Drosophila ortholog. In particular, COUP-TFI is highly expressed in organs that develop by epithelial proliferation and differentiation, including those that develop by mesenchymal differentiation to epithelium.

Mouse COUP-TFI mutants show dose-dependent embryonic lethality or lethality shortly after weaning, reduced growth of the head and heart, severe hemorrhage, edema, enlarged blood vessels, defective angiogenesis, ocular defects, bone defects, and vascular remodeling [ ].

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COUP-TFI mutants are also missing cortical layer IV in the cerebral cortex lamina, due to a failure of axons to extend to their cortical targets, and resulting excessive cell death [ ]—thus a role in neuronal development appears to be evolutionarily-conserved. Defects in the glossopharyngeal nerve result in poor sensation and motor function of the tongue and pharynx, contributing to malnutrition and perinatal death.

The comparison of functions of NR2F family members suggests themes of both exaptation and conservation. A general role in nervous system development is evident among species investigated in detail, but various different roles in organogenesis are apparent in flies and vertebrates.

The estrogen-related receptor ERR gene of Drosophila , although evolutionarily-related to steroid receptors of great interest to human health, has not been fully characterized. This gene class has been lost in nematodes, but is retained in vertebrates Figure 1 , Table 1.


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  • Mutations in ERR are lethal in larval development, indicating that the gene plays an essential function. A recent study showed that ERR is required for normal spermatogenesis in the fly [ ], but the essential function remains undescribed. ERR orthologs are present in Lophotrochozoa and Echinodermata, but were apparently lost from nematode lineages.

    These defects included abnormal heart and spinal cord function [ , ] and developmental defects in early branching events of the ureteric duct of the kidney [ ]. A recent study also described defects in hippocampal neuron physiology and function, but without clear developmental involvement [ ]. Further evidence may clarify a role for ERR orthologs in development, but current studies have revealed scant evidence for conserved functions in ontogeny.

    Drosophila HR38 was identified by molecular cloning as a nuclear receptor with expression associated with morphogenesis [ 19 ]. HR38 does not appear to have a critical role in embryogenesis, but is required for adult cuticle formation during later pupal morphogenesis [ , ].