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1.
Elife ; 122024 Apr 18.
Article in English | MEDLINE | ID: mdl-38634460

ABSTRACT

Mechanosensory neurons located across the body surface respond to tactile stimuli and elicit diverse behavioral responses, from relatively simple stimulus location-aimed movements to complex movement sequences. How mechanosensory neurons and their postsynaptic circuits influence such diverse behaviors remains unclear. We previously discovered that Drosophila perform a body location-prioritized grooming sequence when mechanosensory neurons at different locations on the head and body are simultaneously stimulated by dust (Hampel et al., 2017; Seeds et al., 2014). Here, we identify nearly all mechanosensory neurons on the Drosophila head that individually elicit aimed grooming of specific head locations, while collectively eliciting a whole head grooming sequence. Different tracing methods were used to reconstruct the projections of these neurons from different locations on the head to their distinct arborizations in the brain. This provides the first synaptic resolution somatotopic map of a head, and defines the parallel-projecting mechanosensory pathways that elicit head grooming.


Subject(s)
Drosophila , Neurons , Animals , Grooming/physiology , Afferent Pathways , Neurons/physiology , Brain , Drosophila melanogaster/physiology
2.
bioRxiv ; 2023 Dec 15.
Article in English | MEDLINE | ID: mdl-36798384

ABSTRACT

Mechanosensory neurons located across the body surface respond to tactile stimuli and elicit diverse behavioral responses, from relatively simple stimulus location-aimed movements to complex movement sequences. How mechanosensory neurons and their postsynaptic circuits influence such diverse behaviors remains unclear. We previously discovered that Drosophila perform a body location-prioritized grooming sequence when mechanosensory neurons at different locations on the head and body are simultaneously stimulated by dust (Hampel et al., 2017; Seeds et al., 2014). Here, we identify nearly all mechanosensory neurons on the Drosophila head that individually elicit aimed grooming of specific head locations, while collectively eliciting a whole head grooming sequence. Different tracing methods were used to reconstruct the projections of these neurons from different locations on the head to their distinct arborizations in the brain. This provides the first synaptic resolution somatotopic map of a head, and defines the parallel-projecting mechanosensory pathways that elicit head grooming.

4.
Cell ; 184(2): 507-520.e16, 2021 01 21.
Article in English | MEDLINE | ID: mdl-33382967

ABSTRACT

Aggression involves both sexually monomorphic and dimorphic actions. How the brain implements these two types of actions is poorly understood. We have identified three cell types that regulate aggression in Drosophila: one type is sexually shared, and the other two are sex specific. Shared common aggression-promoting (CAP) neurons mediate aggressive approach in both sexes, whereas functionally downstream dimorphic but homologous cell types, called male-specific aggression-promoting (MAP) neurons in males and fpC1 in females, control dimorphic attack. These symmetric circuits underlie the divergence of male and female aggressive behaviors, from their monomorphic appetitive/motivational to their dimorphic consummatory phases. The strength of the monomorphic → dimorphic functional connection is increased by social isolation in both sexes, suggesting that it may be a locus for isolation-dependent enhancement of aggression. Together, these findings reveal a circuit logic for the neural control of behaviors that include both sexually monomorphic and dimorphic actions, which may generalize to other organisms.


Subject(s)
Aggression/physiology , Drosophila melanogaster/physiology , Logic , Sex Characteristics , Sexual Behavior, Animal/physiology , Animals , Female , Male , Nerve Net/physiology , Neurons/physiology , Social Isolation , Tachykinins/metabolism
5.
Neuron ; 100(6): 1474-1490.e4, 2018 12 19.
Article in English | MEDLINE | ID: mdl-30415997

ABSTRACT

Threat displays are a universal feature of agonistic interactions. Whether threats are part of a continuum of aggressive behaviors or separately controlled remains unclear. We analyze threats in Drosophila and show they are triggered by male cues and visual motion, and comprised of multiple motor elements that can be flexibly combined. We isolate a cluster of ∼3 neurons whose activity is necessary for threat displays but not for other aggressive behaviors, and whose artificial activation suffices to evoke naturalistic threats in solitary flies, suggesting that the neural control of threats is modular with respect to other aggressive behaviors. Artificially evoked threats suffice to repel opponents from a resource in the absence of contact aggression. Depending on its level of artificial activation, this neural threat module can evoke different motor elements in a threshold-dependent manner. Such scalable modules may represent fundamental "building blocks" of neural circuits that mediate complex multi-motor behaviors.


Subject(s)
Aggression/physiology , Behavior, Animal/physiology , Brain/physiology , Motor Activity/physiology , Neurons/physiology , Animals , Animals, Genetically Modified , Brain/cytology , Cues , Drosophila , Drosophila Proteins/genetics , Drosophila Proteins/metabolism , Green Fluorescent Proteins/genetics , Green Fluorescent Proteins/metabolism , Male , Thermogenesis
6.
Neuron ; 95(5): 1112-1128.e7, 2017 Aug 30.
Article in English | MEDLINE | ID: mdl-28858617

ABSTRACT

Diffuse neuromodulatory systems such as norepinephrine (NE) control brain-wide states such as arousal, but whether they control complex social behaviors more specifically is not clear. Octopamine (OA), the insect homolog of NE, is known to promote both arousal and aggression. We have performed a systematic, unbiased screen to identify OA receptor-expressing neurons (OARNs) that control aggression in Drosophila. Our results uncover a tiny population of male-specific aSP2 neurons that mediate a specific influence of OA on aggression, independent of any effect on arousal. Unexpectedly, these neurons receive convergent input from OA neurons and P1 neurons, a population of FruM+ neurons that promotes male courtship behavior. Behavioral epistasis experiments suggest that aSP2 neurons may constitute an integration node at which OAergic neuromodulation can bias the output of P1 neurons to favor aggression over inter-male courtship. These results have potential implications for thinking about the role of related neuromodulatory systems in mammals.


Subject(s)
Aggression/physiology , Drosophila Proteins/physiology , Drosophila/cytology , Drosophila/physiology , Neural Pathways , Neurons/physiology , Receptors, Neurotransmitter/physiology , Social Behavior , Animals , Animals, Genetically Modified , Arousal/physiology , Courtship , Drosophila Proteins/genetics , Interneurons/physiology , Male , Receptors, Neurotransmitter/genetics
7.
Curr Opin Neurobiol ; 38: 109-18, 2016 06.
Article in English | MEDLINE | ID: mdl-27179788

ABSTRACT

Like most animal species, fruit flies fight to obtain and defend resources essential to survival and reproduction. Aggressive behavior in Drosophila is genetically specified and also strongly influenced by the fly's social context, past experiences and internal states, making it an excellent framework for investigating the neural mechanisms that regulate complex social behaviors. Here, I summarize our current knowledge of the neural control of aggression in Drosophila and discuss recent advances in understanding the sensory pathways that influence the decision to fight or court, the neuromodulatory control of aggression, the neural basis by which internal states can influence both fighting and courtship, and how social experience modifies aggressive behavior.


Subject(s)
Aggression/physiology , Drosophila/physiology , Nervous System Physiological Phenomena , Animals , Sexual Behavior, Animal/physiology , Social Behavior
8.
Elife ; 42015 Dec 29.
Article in English | MEDLINE | ID: mdl-26714106

ABSTRACT

How brains are hardwired to produce aggressive behavior, and how aggression circuits are related to those that mediate courtship, is not well understood. A large-scale screen for aggression-promoting neurons in Drosophila identified several independent hits that enhanced both inter-male aggression and courtship. Genetic intersections revealed that 8-10 P1 interneurons, previously thought to exclusively control male courtship, were sufficient to promote fighting. Optogenetic experiments indicated that P1 activation could promote aggression at a threshold below that required for wing extension. P1 activation in the absence of wing extension triggered persistent aggression via an internal state that could endure for minutes. High-frequency P1 activation promoted wing extension and suppressed aggression during photostimulation, whereas aggression resumed and wing extension was inhibited following photostimulation offset. Thus, P1 neuron activation promotes a latent, internal state that facilitates aggression and courtship, and controls the overt expression of these social behaviors in a threshold-dependent, inverse manner.


Subject(s)
Drosophila/physiology , Interneurons/physiology , Aggression , Animals , Courtship , Male , Optogenetics
9.
Cell ; 156(1-2): 221-35, 2014 Jan 16.
Article in English | MEDLINE | ID: mdl-24439378

ABSTRACT

Males of most species are more aggressive than females, but the neural mechanisms underlying this dimorphism are not clear. Here, we identify a neuron and a gene that control the higher level of aggression characteristic of Drosophila melanogaster males. Males, but not females, contain a small cluster of FruM(+) neurons that express the neuropeptide tachykinin (Tk). Activation and silencing of these neurons increased and decreased, respectively, intermale aggression without affecting male-female courtship behavior. Mutations in both Tk and a candidate receptor, Takr86C, suppressed the effect of neuronal activation, whereas overexpression of Tk potentiated it. Tk neuron activation overcame reduced aggressiveness caused by eliminating a variety of sensory or contextual cues, suggesting that it promotes aggressive arousal or motivation. Tachykinin/Substance P has been implicated in aggression in mammals, including humans. Thus, the higher aggressiveness of Drosophila males reflects the sexually dimorphic expression of a neuropeptide that controls agonistic behaviors across phylogeny.


Subject(s)
Drosophila melanogaster/physiology , Neurons/metabolism , Tachykinins/metabolism , Aggression , Animals , Drosophila Proteins/genetics , Drosophila Proteins/metabolism , Female , Male , Mutation , Receptors, Tachykinin/genetics , Receptors, Tachykinin/metabolism , Sex Characteristics
10.
Article in English | MEDLINE | ID: mdl-25948637

ABSTRACT

Social interactions, such as an aggressive encounter between two conspecific males or a mating encounter between a male and a female, typically progress from an initial appetitive or motivational phase, to a final consummatory phase. This progression involves both changes in the intensity of the animals' internal state of arousal or motivation and sequential changes in their behavior. How are these internal states, and their escalating intensity, encoded in the brain? Does this escalation drive the progression from the appetitive/motivational to the consummatory phase of a social interaction and, if so, how are appropriate behaviors chosen during this progression? Recent work on social behaviors in flies and mice suggests possible ways in which changes in internal state intensity during a social encounter may be encoded and coupled to appropriate behavioral decisions at appropriate phases of the interaction. These studies may have relevance to understanding how emotion states influence cognitive behavioral decisions at higher levels of brain function.


Subject(s)
Cognition , Decision Making , Emotions , Social Behavior , Aggression/psychology , Animals , Humans , Neural Pathways/physiology
11.
Nat Methods ; 11(3): 325-32, 2014 Mar.
Article in English | MEDLINE | ID: mdl-24363022

ABSTRACT

Optogenetics allows the manipulation of neural activity in freely moving animals with millisecond precision, but its application in Drosophila melanogaster has been limited. Here we show that a recently described red activatable channelrhodopsin (ReaChR) permits control of complex behavior in freely moving adult flies, at wavelengths that are not thought to interfere with normal visual function. This tool affords the opportunity to control neural activity over a broad dynamic range of stimulation intensities. Using time-resolved activation, we show that the neural control of male courtship song can be separated into (i) probabilistic, persistent and (ii) deterministic, command-like components. The former, but not the latter, neurons are subject to functional modulation by social experience, which supports the idea that they constitute a locus of state-dependent influence. This separation is not evident using thermogenetic tools, a result underscoring the importance of temporally precise control of neuronal activation in the functional dissection of neural circuits in Drosophila.


Subject(s)
Drosophila Proteins/metabolism , Drosophila/physiology , Optogenetics , Rhodopsin/metabolism , Sexual Behavior, Animal/physiology , Animals , Drosophila/genetics , Drosophila Proteins/genetics , Female , Male , Neurons/physiology , Photic Stimulation , Taste Perception
12.
Gen Comp Endocrinol ; 168(2): 209-19, 2010 Sep 01.
Article in English | MEDLINE | ID: mdl-20338173

ABSTRACT

Corticosteroids (CS) act synergistically with thyroid hormone (TH) to accelerate amphibian metamorphosis. Earlier studies showed that CS increase nuclear 3,5,3'-triiodothyronine (T(3)) binding capacity in tadpole tail, and 5' deiodinase activity in tadpole tissues, increasing the generation of T(3) from thyroxine (T(4)). In the present study we investigated CS synergy with TH by analyzing expression of key genes involved in TH and CS signaling using tadpole tail explant cultures, prometamorphic tadpoles, and frog tissue culture cells (XTC-2 and XLT-15). Treatment of tail explants with T(3) at 100 nM, but not at 10 nM caused tail regression. Corticosterone (CORT) at three doses (100, 500 and 3400 nM) had no effect or increased tail size. T(3) at 10 nM plus CORT caused tails to regress similar to 100 nM T(3). Thyroid hormone receptor beta (TRbeta) mRNA was synergistically upregulated by T(3) plus CORT in tail explants, tail and brain in vivo, and tissue culture cells. The activating 5' deiodinase type 2 (D2) mRNA was induced by T(3) and CORT in tail explants and tail in vivo. Thyroid hormone increased expression of glucocorticoid (GR) and mineralocorticoid receptor (MR) mRNAs. Our findings support that the synergistic actions of TH and CS in metamorphosis occur at the level of expression of genes for TRbeta and D2, enhancing tissue sensitivity to TH. Concurrently, TH enhances tissue sensitivity to CS by upregulating GR and MR. Environmental stressors can modulate the timing of tadpole metamorphosis in part by CS enhancing the response of tadpole tissues to the actions of TH.


Subject(s)
Adrenal Cortex Hormones/pharmacology , Larva/growth & development , Metamorphosis, Biological/drug effects , Triiodothyronine/pharmacology , Xenopus/growth & development , Animals , Cell Line , Drug Synergism , In Vitro Techniques , Larva/drug effects , Reverse Transcriptase Polymerase Chain Reaction
13.
Nat Methods ; 6(4): 297-303, 2009 Apr.
Article in English | MEDLINE | ID: mdl-19270697

ABSTRACT

We introduce a method based on machine vision for automatically measuring aggression and courtship in Drosophila melanogaster. The genetic and neural circuit bases of these innate social behaviors are poorly understood. High-throughput behavioral screening in this genetically tractable model organism is a potentially powerful approach, but it is currently very laborious. Our system monitors interacting pairs of flies and computes their location, orientation and wing posture. These features are used for detecting behaviors exhibited during aggression and courtship. Among these, wing threat, lunging and tussling are specific to aggression; circling, wing extension (courtship 'song') and copulation are specific to courtship; locomotion and chasing are common to both. Ethograms may be constructed automatically from these measurements, saving considerable time and effort. This technology should enable large-scale screens for genes and neural circuits controlling courtship and aggression.


Subject(s)
Artificial Intelligence , Behavior, Animal/physiology , Drosophila melanogaster/anatomy & histology , Drosophila melanogaster/physiology , Image Interpretation, Computer-Assisted/methods , Monitoring, Physiologic/methods , Social Behavior , Animals , Humans , Movement/physiology , Pattern Recognition, Automated/methods , Posture/physiology
14.
J Neurosci ; 28(24): 6092-103, 2008 Jun 11.
Article in English | MEDLINE | ID: mdl-18550751

ABSTRACT

Drosophila mushroom body (MB) gamma neurons undergo axon pruning during metamorphosis through a process of localized degeneration of specific axon branches. Developmental axon degeneration is initiated by the steroid hormone ecdysone, acting through a nuclear receptor complex composed of USP (ultraspiracle) and EcRB1 (ecdysone receptor B1) to regulate gene expression in MB gamma neurons. To identify ecdysone-dependent gene expression changes in MB gamma neurons at the onset of axon pruning, we use laser capture microdissection to isolate wild-type and mutant MB neurons in which EcR (ecdysone receptor) activity is genetically blocked, and analyze expression changes by microarray. We identify several molecular pathways that are regulated in MB neurons by ecdysone. The most striking observation is the upregulation of genes involved in the UPS (ubiquitin-proteasome system), which is cell autonomously required for gamma neuron pruning. In addition, we characterize the function of Boule, an evolutionarily conserved RNA-binding protein previously implicated in spermatogenesis in flies and vertebrates. boule expression is downregulated by ecdysone in MB neurons at the onset of pruning, and forced expression of Boule in MB gamma neurons is sufficient to inhibit axon pruning. This activity is dependent on the RNA-binding domain of Boule and a conserved DAZ (deleted in azoospermia) domain implicated in interactions with other RNA-binding proteins. However, loss of Boule does not result in obvious defects in axon pruning or morphogenesis of MB neurons, suggesting that it acts redundantly with other ecdyonse-regulated genes. We propose a novel function for Boule in the CNS as a negative regulator of developmental axon pruning.


Subject(s)
Axons/physiology , Drosophila Proteins/physiology , Genomics/methods , Mushroom Bodies/cytology , Neurons/cytology , RNA-Binding Proteins/physiology , Animals , Animals, Genetically Modified , CD8 Antigens/genetics , CD8 Antigens/metabolism , Drosophila , Drosophila Proteins/genetics , Drosophila Proteins/metabolism , Ecdysone/pharmacology , Gene Expression Regulation, Developmental/drug effects , Gene Expression Regulation, Developmental/physiology , Green Fluorescent Proteins/genetics , Green Fluorescent Proteins/metabolism , Larva , Microarray Analysis/methods , Mutation , Neurons/physiology , Receptors, Steroid/metabolism
15.
Neuron ; 50(6): 883-95, 2006 Jun 15.
Article in English | MEDLINE | ID: mdl-16772170

ABSTRACT

Axon pruning by degeneration remodels exuberant axonal connections and is widely required for the development of proper circuitry in the nervous system from insects to mammals. Developmental axon degeneration morphologically resembles injury-induced Wallerian degeneration, suggesting similar underlying mechanisms. As previously reported for mice, we show that Wlds protein substantially delays Wallerian degeneration in flies. Surprisingly, Wlds has no effect on naturally occurring developmental axon degeneration in flies or mice, although it protects against injury-induced degeneration of the same axons at the same developmental age. By contrast, the ubiquitin-proteasome system is intrinsically required for both developmental and injury-induced axon degeneration. We also show that the glial cell surface receptor Draper is required for efficient clearance of axon fragments during developmental axon degeneration, similar to its function in injury-induced degeneration. Thus, mechanistically, naturally occurring developmental axon pruning by degeneration and injury-induced axon degeneration differ significantly in early steps, but may converge onto a common execution pathway.


Subject(s)
Axons/physiology , Drosophila Proteins/physiology , Gene Expression Regulation, Developmental/physiology , Nerve Tissue Proteins/physiology , Wallerian Degeneration/metabolism , Animals , Animals, Genetically Modified , Axons/metabolism , Axons/ultrastructure , Drosophila , Drosophila Proteins/biosynthesis , Drosophila Proteins/genetics , Mice , Mice, Inbred C57BL , Nerve Tissue Proteins/biosynthesis , Nerve Tissue Proteins/genetics , Wallerian Degeneration/genetics , Wallerian Degeneration/pathology
16.
Neuron ; 39(2): 217-25, 2003 Jul 17.
Article in English | MEDLINE | ID: mdl-12873380

ABSTRACT

Local axon degeneration is a common pathological feature of many neurodegenerative diseases and peripheral neuropathies. While it is believed to operate with an apoptosis-independent molecular program, the underlying molecular mechanisms are largely unknown. In this study, we used the degeneration of transected axons, termed "Wallerian degeneration," as a model to examine the possible involvement of the ubiquitin proteasome system (UPS). Inhibiting UPS activity by both pharmacological and genetic means profoundly delays axon degeneration both in vitro and in vivo. In addition, we found that the fragmentation of microtubules is the earliest detectable change in axons undergoing Wallerian degeneration, which among other degenerative events, can be delayed by proteasome inhibitors. Interestingly, similar to transected axons, degeneration of axons from nerve growth factor (NGF)-deprived sympathetic neurons could also be suppressed by proteasome inhibitors. Our findings suggest a possibility that inhibiting UPS activity may serve to retard axon degeneration in pathological conditions.


Subject(s)
Cysteine Endopeptidases/metabolism , Multienzyme Complexes/metabolism , Ubiquitin/metabolism , Wallerian Degeneration/metabolism , Amino Acids/pharmacokinetics , Animals , Animals, Newborn , Axons/chemistry , Benzimidazoles/pharmacokinetics , Blotting, Western , Calpain/metabolism , Cells, Cultured , Chelating Agents/pharmacology , Cysteine Proteinase Inhibitors/pharmacology , Cytoskeleton/metabolism , Disease Models, Animal , Drug Interactions , Egtazic Acid/pharmacology , Endopeptidases/metabolism , Ganglia, Sympathetic/drug effects , Ganglia, Sympathetic/metabolism , Ganglia, Sympathetic/virology , Immunohistochemistry , Leupeptins/therapeutic use , Microtubules/metabolism , Nerve Growth Factor/metabolism , Optic Nerve/physiology , Optic Nerve Injuries/metabolism , Peptide Fragments/metabolism , Proteasome Endopeptidase Complex , Rats , Time Factors , Tubulin/metabolism , Wallerian Degeneration/physiopathology , Wallerian Degeneration/prevention & control
17.
Neuron ; 38(6): 871-85, 2003 Jun 19.
Article in English | MEDLINE | ID: mdl-12818174

ABSTRACT

Axon pruning is widely used for the refinement of neural circuits in both vertebrates and invertebrates, and may also contribute to the pathogenesis of neurodegenerative diseases. However, little is known about the cellular and molecular mechanisms of axon pruning. We use the stereotyped pruning of gamma neurons of the Drosophila mushroom bodies (MB) during metamorphosis to investigate these mechanisms. Detailed time course analyses indicate that MB axon pruning is mediated by local degeneration rather than retraction and that the disruption of the microtubule cytoskeleton precedes axon pruning. In addition, multiple lines of genetic evidence demonstrate an intrinsic role of the ubiquitin-proteasome system in axon pruning; for example, loss-of-function mutations of the ubiquitin activating enzyme (E1) or proteasome subunits in MB neurons block axon pruning. Our findings suggest that some forms of axon pruning during development may share similarities with degeneration of axons in response to injury.


Subject(s)
Axons/physiology , Cysteine Endopeptidases/physiology , Drosophila/growth & development , Drosophila/ultrastructure , Metamorphosis, Biological/physiology , Multienzyme Complexes/physiology , Ubiquitin/physiology , Animals , Axons/ultrastructure , Cell Adhesion Molecules/analysis , Cytoskeletal Proteins/analysis , Cytoskeleton/ultrastructure , Cytosol/chemistry , Drosophila/genetics , Endocytosis , Endopeptidases/genetics , Gene Expression , Ligases/genetics , Ligases/physiology , Microtubules/ultrastructure , Mutation , Nerve Degeneration , Neurons/metabolism , Neurons/ultrastructure , Proteasome Endopeptidase Complex , Saccharomyces cerevisiae/enzymology , Synapses/chemistry , Transfection , Ubiquitin-Activating Enzymes , Ubiquitin-Protein Ligases
18.
Dev Growth Differ ; 44(5): 365-81, 2002 Oct.
Article in English | MEDLINE | ID: mdl-12392570

ABSTRACT

Basic transcription element binding protein (BTEB) is a member of the Krüppel family of zinc finger transcription factors. It has been shown that BTEB plays a role in promoting neuronal process formation during postembryonic development. In the present study, the biochemical properties, transactivation function, and the developmental and hormone-regulated expression of BTEB in Xenopus laevis (xBTEB) are described. xBTEB binds the GC-rich basic transcription element (BTE) with high affinity and functions as a transcriptional activator on promoters containing multiple or single GC boxes. xBTEB mRNA levels increase in the tadpole brain, intestine and tail during metamorphosis, and are correlated with tissue-specific morphological and biochemical transformations. xBTEB mRNA expression can be induced precociously in premetamorphic tadpole tissues by treatment with thyroid hormone. In situ hybridization histochemistry showed that thyroid hormone upregulates xBTEB mRNA throughout the brain of premetamorphic tadpoles, with the highest expression found in the subventricular zones of the telencephalon, diencephalon, optic tectum, cerebellum and spinal cord. xBTEB protein parallels changes in its mRNA, and it was found that xBTEB is not expressed in mitotic cells in the developing brain, but is expressed just distal to the proliferative zone, supporting the hypothesis that this protein plays a role in neural cell differentiation.


Subject(s)
DNA-Binding Proteins/genetics , Metamorphosis, Biological/physiology , Transcription Factors/genetics , Xenopus Proteins , Animals , Blotting, Northern , Brain/immunology , Brain/metabolism , Cell Division/physiology , DNA-Binding Proteins/biosynthesis , DNA-Binding Proteins/immunology , DNA-Binding Proteins/metabolism , Kruppel-Like Transcription Factors , Metamorphosis, Biological/genetics , Promoter Regions, Genetic , Rats , Receptors, Thyroid Hormone/metabolism , Transcription Factors/biosynthesis , Transcription Factors/immunology , Transcription Factors/metabolism , Triiodothyronine/metabolism , Up-Regulation , Xenopus laevis
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