C. Elegans Model for Studying Tropomyosin and Troponin Regulations of Muscle Contraction and Animal Behavior

ABSTRACTCoordinated rhythmic movements are ubiquitous in animal behavior. In many organisms, chains of neural oscillators underlie the generation of these rhythms. In C. elegans, locomotor wave generation has been poorly understood; in particular, it is unclear where in the circuit rhythms are generated, and whether there exists more than one such generator. We used optogenetic and ablation experiments to probe the nature of rhythm generation in the locomotor circuit. We found that multiple sections of forward locomotor circuitry are capable of independently generating rhythms. By perturbing different components of the motor circuit, we localize the source of secondary rhythms to cholinergic motor neurons in the midbody. Using rhythmic optogenetic perturbation we demonstrate bidirectional entrainment of oscillations between different body regions. These results show that, as in many other vertebrates and invertebrates, the C. elegans motor circuit contains multiple oscillators that coordinate activity to generate behavior.

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A microfluidic-induced C. elegans sleep state

Nature Communications ◽

10.1038/s41467-019-13008-5 ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 7

Author(s):

Daniel L. Gonzales ◽

Jasmine Zhou ◽

Bo Fan ◽

Jacob T. Robinson

Keyword(s):

Animal Behavior ◽

Animal Movement ◽

Quiescent State ◽

Sleep State ◽

C Elegans ◽

Sensory Pathways ◽

Simultaneous Control ◽

Behavioral Requirements ◽

Microfluidic Chambers ◽

The Brain

Abstract An important feature of animal behavior is the ability to switch rapidly between activity states, however, how the brain regulates these spontaneous transitions based on the animal’s perceived environment is not well understood. Here we show a C. elegans sleep-like state on a scalable platform that enables simultaneous control of multiple environmental factors including temperature, mechanical stress, and food availability. This brief quiescent state, which we refer to as microfluidic-induced sleep, occurs spontaneously in microfluidic chambers, which allows us to track animal movement and perform whole-brain imaging. With these capabilities, we establish that microfluidic-induced sleep meets the behavioral requirements of C. elegans sleep and depends on multiple factors, such as satiety and temperature. Additionally, we show that C. elegans sleep can be induced through mechanosensory pathways. Together, these results establish a model system for studying how animals process multiple sensory pathways to regulate behavioral states.

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C. elegans episodic swimming is driven by multifractal kinetics

10.1101/2020.04.22.056606 ◽

2020 ◽

Author(s):

Yusaku Ikeda ◽

Peter Jurica ◽

Hiroshi Kimura ◽

Hiroaki Takagi ◽

Struzik Zbigniew ◽

...

Keyword(s):

Animal Behavior ◽

Common Property ◽

Molecular Mechanisms ◽

Temporal Change ◽

Temporal Correlation ◽

Liquid Solution ◽

Fractal Nature ◽

Fractal Scaling ◽

Scale Free ◽

C Elegans

AbstractFractal scaling is a common property of temporal change in various modes of animal behavior. The molecular mechanisms of fractal scaling in animal behaviors remain largely unexplored. The nematode C. elegans alternates between swimming and resting states in a liquid solution. Here, we report that C. elegans episodic swimming is characterized by scale-free kinetics with long-range temporal correlation and local temporal clusterization, which is characterized as multifractal kinetics. Residence times in actively-moving and inactive states were distributed in a power law-based scale-free manner. Multifractal analysis showed that temporal correlation and temporal clusterization were distinct between the actively-moving state and the inactive state. These results indicate that C. elegans episodic swimming is driven by transition between two behavioral states, in which each of two transition kinetics follows distinct multifractal kinetics. We found that a conserved behavioral modulator, cyclic GMP dependent kinase (PKG) may regulate the multifractal kinetics underlying an animal behavior. Our combinatorial analysis approach involving molecular genetics and kinetics provides a platform for the molecular dissection of the fractal nature of physiological and behavioral phenomena.

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A Regulatory Loop between the Retinoid-Related Orphan Nuclear Receptor NHR-23 and let-7 family microRNAs Modulates the C. elegans Molting Cycle

10.1101/506261 ◽

2018 ◽

Cited By ~ 2

Author(s):

Ruhi Patel ◽

Alison R Frand

Keyword(s):

Animal Behavior ◽

Feedback Loop ◽

Feedback Loops ◽

Biological Clocks ◽

Orphan Nuclear Receptor ◽

Molting Cycle ◽

C Elegans ◽

Animal Physiology ◽

Core Components ◽

Regulatory Loop

Animal physiology and development both rely on biological clocks, but the extent to which feedback loops among core components of the circadian clock and conserved microRNAs operate within developmental timers is not well understood. Here, we show that a negative feedback loop between NHR-23/RORα and let-7 modulates the PER dependent rhythm of the C. elegans molting cycle. Related quiescent intervals are delayed and protracted in nhr-23 knockdowns, advanced and abbreviated in particular let-7 mutants, and yet scheduled more regularly in double mutants. NHR-23 binds upstream ROR Response Elements (REs) and activates transcription of primary let-7 when larvae are active, whereas let-7 targets an LCS in the 3′UTR and represses expression of nhr-23 transcripts when larvae are quiescent. Moreover, NHR-23 and let-7 have scores of shared targets that are cyclically expressed and mediate related transitions in cell and animal behavior. ROREs are also found upstream of vertebrate let-7 homologs, while LCSs are found in 3′UTRs of ROR transcripts. Conservation of this feedback loop has implications for human clocks and related malignancies and disorders of sleep and metabolism.

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unc-68 encodes a ryanodine receptor involved in regulating C. elegans body-wall muscle contraction.

The Journal of Cell Biology ◽

10.1083/jcb.134.4.885 ◽

1996 ◽

Vol 134 (4) ◽

pp. 885-893 ◽

Cited By ~ 84

Author(s):

E B Maryon ◽

R Coronado ◽

P Anderson

Keyword(s):

Muscle Contraction ◽

Ryanodine Receptor ◽

Body Wall ◽

Striated Muscle ◽

Ryanodine Receptors ◽

Binding Activity ◽

Body Wall Muscle ◽

Calcium Signal ◽

C Elegans ◽

Muscle Ultrastructure

Striated muscle contraction is elicited by the release of stored calcium ions through ryanodine receptor channels in the sarcoplasmic reticulum. ryr-1 is a C. elegans ryanodine receptor homologue that is expressed in body-wall muscle cells used for locomotion. Using genetic methods, we show that ryr-1 is the previously identified locus unc-68. First, transposon-induced deletions within ryr-1 are alleles of unc-68. Second, transformation of unc-68 mutants with ryr-1 genomic DNA results in rescue of the Unc phenotype. unc-68 mutants move poorly, exhibiting an incomplete flaccid paralysis, yet have normal muscle ultrastructure. The mutants are insensitive to the paralytic effects of ryanodine, and lack detectable ryanodine-binding activity. The Unc-68 phenotype suggests that ryanodine receptors are not essential for excitation-contraction coupling in nematodes, but act to amplify a (calcium) signal that is sufficient for contraction.

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Faculty Opinions recommendation of Protons act as a transmitter for muscle contraction in C. elegans.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1099249.555473 ◽

2008 ◽

Author(s):

Silvana Curci

Keyword(s):

Muscle Contraction ◽

C Elegans

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PKN-1, a Homologue of Mammalian PKN, Is Involved in the Regulation of Muscle Contraction and Force Transmission in C. elegans

Journal of Molecular Biology ◽

10.1016/j.jmb.2011.01.039 ◽

2011 ◽

Vol 407 (2) ◽

pp. 222-231 ◽

Cited By ~ 5

Author(s):

Hiroshi Qadota ◽

Takayuki Miyauchi ◽

John F. Nahabedian ◽

Jeffrey N. Stirman ◽

Hang Lu ◽

...

Keyword(s):

Muscle Contraction ◽

Force Transmission ◽

C Elegans ◽

Regulation Of Muscle Contraction

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Typical action potentials drive muscle contraction in C. elegans

Frontiers in Neuroscience ◽

10.3389/conf.neuro.03.2009.17.016 ◽

2009 ◽

Vol 3 ◽

Author(s):

Zhen Mei

Keyword(s):

Muscle Contraction ◽

Action Potentials ◽

C Elegans ◽

Typical Action

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The female-specific VC neurons are mechanically activated, feed-forward motor neurons that facilitate serotonin-induced egg laying in C. elegans

10.1101/2020.08.11.246942 ◽

2020 ◽

Author(s):

Richard J. Kopchock ◽

Bhavya Ravi ◽

Addys Bode ◽

Kevin M. Collins

Keyword(s):

Muscle Contraction ◽

Motor Neurons ◽

Neural Circuit ◽

Egg Laying ◽

Muscle Contractility ◽

C Elegans ◽

Optogenetic Stimulation ◽

Vulval Muscle ◽

Female Specific ◽

Stimulation Of

AbstractSuccessful execution of behavior requires the coordinated activity and communication between multiple cell types. Studies using the relatively simple neural circuits of invertebrates have helped to uncover how conserved molecular and cellular signaling events shape animal behavior. To understand the mechanisms underlying neural circuit activity and behavior, we have been studying a simple circuit that drives egg-laying behavior in the nematode worm C. elegans. Here we show that the female-specific, Ventral C (VC) motoneurons are required for vulval muscle contractility and egg laying in response to serotonin. Ca2+ imaging experiments show the VCs are active during times of vulval muscle contraction and vulval opening, and optogenetic stimulation of the VCs promotes vulval muscle Ca2+ activity. However, while silencing of the VCs does not grossly affect steady-state egg-laying behavior, VC silencing does block egg laying in response to serotonin and increases the failure rate of egg-laying attempts. Signaling from the VCs facilitates full vulval muscle contraction and opening of the vulva for efficient egg laying. We also find the VCs are mechanically activated in response to vulval opening. Optogenetic stimulation of the vulval muscles is sufficient to drive VC Ca2+ activity and requires muscle contractility, showing the presynaptic VCs and the postsynaptic vulval muscles can mutually excite each other. Together, our results demonstrate that the VC neurons facilitate efficient execution of egg-laying behavior by coordinating postsynaptic muscle contractility in response to serotonin and mechanosensory feedback.

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C. elegans episodic swimming is driven by multifractal kinetics

Scientific Reports ◽

10.1038/s41598-020-70319-0 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Yusaku Ikeda ◽

Peter Jurica ◽

Hiroshi Kimura ◽

Hiroaki Takagi ◽

Zbigniew R. Struzik ◽

...

Keyword(s):

Animal Behavior ◽

Common Property ◽

Molecular Mechanisms ◽

Temporal Change ◽

Temporal Correlation ◽

Liquid Solution ◽

Fractal Nature ◽

Fractal Scaling ◽

Scale Free ◽

C Elegans

Abstract Fractal scaling is a common property of temporal change in various modes of animal behavior. The molecular mechanisms of fractal scaling in animal behaviors remain largely unexplored. The nematode C. elegans alternates between swimming and resting states in a liquid solution. Here, we report that C. elegans episodic swimming is characterized by scale-free kinetics with long-range temporal correlation and local temporal clusterization, namely consistent with multifractal kinetics. Residence times in actively-moving and inactive states were distributed in a power law-based scale-free manner. Multifractal analysis showed that temporal correlation and temporal clusterization were distinct between the actively-moving state and the inactive state. These results indicate that C. elegans episodic swimming is driven by transition between two behavioral states, in which each of two transition kinetics follows distinct multifractal kinetics. We found that a conserved behavioral modulator, cyclic GMP dependent kinase (PKG) may regulate the multifractal kinetics underlying an animal behavior. Our combinatorial analysis approach involving molecular genetics and kinetics provides a platform for the molecular dissection of the fractal nature of physiological and behavioral phenomena.

Download Full-text