A Single Gene Target of an ETS-Family Transcription Factor Determines Neuronal CO2-Chemosensitivity

Brandt, Julia P.; Aziz-Zaman, Sonya; Juozaityte, Vaida; Martínez-Velázquez, Luis A.; Petersen, Jakob Gramstrup; Pocock, Roger; Ringstad, Niels

doi:10.1371/journal.pone.0034014

Cited by 39 publications

(77 citation statements)

References 40 publications

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“…The ASG neurons are also able to act in stress conditions when they are recruited to a novel neuronal circuit to enable an escape response (52). In contrast, the BAG neurons function to detect changes in oxygen and carbon dioxide in the environment and to coordinate behavioral responses according to changes in environmental gas status (26,(53)(54)(55)(56). Our behavioral state analysis shows that the ASG and BAG neurons are both important for the inhibition of quiescence under standard laboratory conditions, whereas the ASG neurons potentially play a more major role in the inhibition of roaming behavior.…”

Section: Discussionmentioning

confidence: 99%

“…The transcriptional targets of ETS-5 in the ASG and BAG neurons have not been fully described; however, previous studies have shown that specific FMRFamide-related neuropeptides, expressed in the BAG neurons (FLP-13 and FLP-19), are regulated by ETS-5 (26,27). Therefore, we examined the behavior of mutant strains lacking these neuropeptides, and found that loss of both flp-13 and flp-19 caused a partial decrease in exploratory capacity.…”

Section: Neuropeptide Signaling Contributes To the Control Of Exploramentioning

confidence: 95%

“…Previous studies have shown that ETS-5 specifies the oxygen-and carbon dioxide-sensing neuron fate of the BAG neurons (26,27). ETS-5 is required for BAG expression of the CO 2 -sensing receptor-type guanylate cyclase GCY-9 and the O 2 -sensing soluble guanylate cyclases GCY-31 and GCY-33.…”

Section: Ets-5 Mutant Defects In Oxygen-and Carbon Dioxide-sensingmentioning

confidence: 97%

“…As such, ets-5 mutant animals are unable to coordinate behavioral responses to CO 2 exposure or to downsteps in O 2 levels ( Fig. S1 B and C) (26,27). We tested whether these deficits in O 2 -and CO 2 -sensing function in ets-5 mutant animals may be responsible for their reduced exploratory capacity.…”

Section: Ets-5 Mutant Defects In Oxygen-and Carbon Dioxide-sensingmentioning

confidence: 99%

“…Members of the ETS TF family are functionally diverse; in C. elegans, for example, AST-1/ETV1 regulates axon guidance and dopaminergic neuron differentiation (22,23), LIN-1/ELK3 regulates vulval development downstream of MAP kinase signaling (24), and ETS-4/SPDEF controls lifespan (25). We and others have previously shown that ETS-5/FEV controls the carbon dioxide-sensing function of the BAG neurons (26,27). In vertebrates, the homologs of ETS-5, FEV(human)/Pet1(mouse), also play prominent roles in brain development and function, including the control of circadian rhythms, as well as anxiety-like and aggressive behaviors (28)(29)(30).…”

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The ETS-5 transcription factor regulates activity states in Caenorhabditis elegans by controlling satiety

Juozaityte

Pladevall‐Morera

Podolska

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Animal behavior is shaped through interplay among genes, the environment, and previous experience. As in mammals, satiety signals induce quiescence in Caenorhabditis elegans. Here we report that the C. elegans transcription factor ETS-5, an ortholog of mammalian FEV/Pet1, controls satiety-induced quiescence. Nutritional status has a major influence on C. elegans behavior. When foraging, food availability controls behavioral state switching between active (roaming) and sedentary (dwelling) states; however, when provided with high-quality food, C. elegans become sated and enter quiescence. We show that ETS-5 acts to promote roaming and inhibit quiescence by setting the internal "satiety quotient" through fat regulation. Acting from the ASG and BAG sensory neurons, we show that ETS-5 functions in a complex network with serotonergic and neuropeptide signaling pathways to control food-regulated behavioral state switching. Taken together, our results identify a neuronal mechanism for controlling intestinal fat stores and organismal behavioral states in C. elegans, and establish a paradigm for the elucidation of obesity-relevant mechanisms.ETS transcription factor | neuronal signaling | satiety | fat levels | quiescence A nimal behavior is strongly influenced by the availability of food. In invertebrates and vertebrates, appetite, locomotor activity, and sleep rhythms are all driven by nutritional state (1-7). When malnourished, animals seek out a new food source by actively exploring their environment (roaming), whereas animals that are well fed tend to explore less (dwelling) and when fully sated enter a quiescent or sleep-like state (1-3, 8, 9). Transitions between these behavioral states can be regulated by sensory perception of external stimuli and through gut signals or other internal cues that are generated according to food quality (3,4,6).Initial evidence for neuronal regulation of feeding behavior was shown in mammals using hypothalamic lesions (10). Sectioning of specific regions within the rat hypothalamus evoked opposing behaviors. Removal of one section caused overeating and obesity, whereas removal of an adjacent section resulted in starvation owing to reduced eating (10). Subsequent studies showed that the pro-opiomelanocortin-expressing neurons in the hypothalamus function to suppress feeding, whereas a hypothalamic region that contains neuropeptide Y/agouti-related protein-expressing neurons promotes feeding (11). These adjacent brain regions integrate signals received from the gut that report satiety (12). The nutritive content of food itself also serves as a potent regulator of behavior. In mammals, a diet loaded with fats and sugars stimulates overfeeding and leads to obesity (13). In addition, rats can learn to select a source of food based exclusively on its nutritional value in the absence of external cues (14).In Caenorhabditis elegans, as in mammals, nutritive value is a behavioral stimulus (1, 4). Nematodes exhibit different behaviors when cultured on low-quality food compared to high-quality...

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Section: Discussionmentioning

confidence: 99%

Section: Neuropeptide Signaling Contributes To the Control Of Exploramentioning

confidence: 95%

Section: Ets-5 Mutant Defects In Oxygen-and Carbon Dioxide-sensingmentioning

confidence: 97%

Section: Ets-5 Mutant Defects In Oxygen-and Carbon Dioxide-sensingmentioning

confidence: 99%

mentioning

confidence: 99%

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The ETS-5 transcription factor regulates activity states in Caenorhabditis elegans by controlling satiety

Juozaityte

Pladevall‐Morera

Podolska

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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A map of terminal regulators of neuronal identity in Caenorhabditis elegans

Hobert

2016

WIREs Developmental Biology

113

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Our present day understanding of nervous system development is an amalgam of insights gained from studying different aspects and stages of nervous system development in a variety of invertebrate and vertebrate model systems, with each model system making its own distinctive set of contributions. One aspect of nervous system development that has been among the most extensively studied in the nematode C. elegans is the nature of the gene regulatory programs that specify hardwired, terminal cellular identities. I will first summarize a number of maps (anatomical, functional, molecular) that describe the terminal identity of individual neurons in the C. elegans nervous system. I then provide a comprehensive summary of regulatory factors that specify terminal identities in the nervous system, synthesizing these past studies into a regulatory map of cellular identities in the C. elegans nervous system. This map shows that for three quarters of all neurons in the C. elegans nervous system, regulatory factors that control terminal identity features are known. In-depth studies of specific neuron types have revealed that regulatory factors rarely act alone, but rather act cooperatively in neuron-type specific combinations. In most cases examined so far, distinct, biochemically-unlinked terminal identity features are co-regulated via cooperatively acting transcription factors, termed terminal selectors, but there are also cases in which distinct identity features are controlled in a piecemeal fashion by independent regulatory inputs. The regulatory map also illustrates that identity-defining transcription factors are re-employed in distinct combinations in different neuron types. However, the same transcription factor can drive terminal differentiation in neurons that are unrelated by lineage, unrelated by function, connectivity and neurotransmitter deployment. Lastly, the regulatory map illustrates the preponderance of homeodomain transcription factors in the control of terminal identities, suggesting that these factors have ancient, phylogenetically conserved roles in controlling terminal neuronal differentiation in the nervous system.

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The neurobiology of sensing respiratory gases for the control of animal behavior

Dengke

Ringstad

2012

Front. Biol.

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Aerobic metabolism is fundamental for almost all animal life. Cellular consumption of oxygen (O2) and production of carbon dioxide (CO2) signal metabolic states and physiological stresses. These respiratory gases are also detected as environmental cues that can signal external food quality and the presence of prey, predators and mates. In both contexts, animal nervous systems are endowed with mechanisms for sensing O2/CO2 to trigger appropriate behaviors and maintain homeostasis of internal O2/CO2. Although different animal species show different behavioral responses to O2/CO2, some underlying molecular mechanisms and pathways that function in the detection of respiratory gases are fundamentally similar and evolutionarily conserved. Studies of Caenorhabditis elegans and Drosophila melanogaster have identified roles for cyclic nucleotide signaling and the hypoxia inducible factor (HIF) transcriptional pathway in mediating behavioral responses to respiratory gases. Understanding how simple invertebrate nervous systems detect respiratory gases to control behavior might reveal general principles common to nematodes, insects and vertebrates that function in the molecular sensing of respiratory gases and the neural control of animal behaviors.

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A Single Gene Target of an ETS-Family Transcription Factor Determines Neuronal CO2-Chemosensitivity

Cited by 39 publications

References 40 publications

The ETS-5 transcription factor regulates activity states in Caenorhabditis elegans by controlling satiety

The ETS-5 transcription factor regulates activity states in Caenorhabditis elegans by controlling satiety

A map of terminal regulators of neuronal identity in Caenorhabditis elegans

The neurobiology of sensing respiratory gases for the control of animal behavior

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