Contribution of the cyclic nucleotide gated channel subunit, CNG-3, to olfactory plasticity in Caenorhabditis elegans

O'Halloran, Damien M.; Altshuler-Keylin, Svetlana; Zhang, Xiao Dong; He, Chao; Morales-Phan, Christopher; Yu, Yawei; Kaye, Julia; Brueggemann, Chantal; Chen, Tsung‐Yu; L’Étoile, Noëlle D.

doi:10.1038/s41598-017-00126-7

Cited by 23 publications

(35 citation statements)

References 43 publications

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“…The inability of bm-tax-4 or bm-osm-9 to rescue chemotaxis defects in C. elegans knockouts suggest that these heterologously expressed genes are unable to form homomeric channels or heteromeric channels with endogenous C. elegans subunits that function in a homologous manner. The clade IIIc loss of CNGs involved in olfactory plasticity ( cng-1 , cng-3 ) and TRPs that are expressed in the mechanosensory labial QLQ neurons of C. elegans ( ocr-4 , trpa-1 ) indicate that there is not perfect conservation of all sensory modalities between C. elegans and filarial nematodes, and it is possible that filarial nematode TRP and CNG channels have evolved subunit interactions or primary functions that are not conserved in C. elegans (30,51,82,83) .…”

Section: Discussionmentioning

confidence: 99%

Genetic and functional diversification of chemosensory pathway receptors in mosquito-borne filarial nematodes

Wheeler

Heimark

Airs

et al. 2019

Preprint

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Lymphatic filariasis (LF) afflicts over 60 million people worldwide and leads to severe pathological outcomes in chronic cases. The filarial nematode parasites that cause LF require both arthropod (mosquito) intermediate hosts and mammalian definitive hosts for their propagation. The invasion and migration of filarial parasites through host tissues are complex and critical to survival, yet little is known about the receptors and signaling pathways that mediate taxis in these medically important species.To better understand filarial chemosensation we employ comparative genomics, transcriptomics, reverse genetics, and chemical approaches to identify putative chemosensory receptor proteins and perturb chemosensory phenotypes in filarial nematode parasites. We find that chemoreceptor family size is correlated with the presence of environmental (extra-host) stages in nematode life cycles, and that filarial parasites contain a compact and highly-diverged chemoreceptor complement and lineage-specific ion channels that are predicted to operate downstream of chemoreceptor activation. In Brugia malayi, an etiological agent of LF, chemoreceptor expression patterns correspond to distinct parasite migration events across the life cycle. To interrogate the role of chemosensation in host migration, arthropod infectious stage (microfilariae) and vertebrate infectious stage (L3) Brugia parasites were incubated in nicotinamide, an agonist of the nematode transient receptor potential (TRP) channel osm-9 . Exposure of microfilariae to nicotinamide alters intra-mosquito migration while exposure of L3s reduces chemotaxis towards host-associated cues in vitro . Nicotinamide exposure also modulates thermosensory responses in L3s, suggesting a polymodal sensory role for Brugia osm-9 . Reverse genetic studies implicate both osm-9 and the cyclic nucleotide-gated (CNG) channel subunit tax-4 in larval chemotaxis towards host serum, while these ion channel subunits do not rescue chemosensory defects in C. elegans osm-9 and tax-4 knock-out strains. Together, these data reveal genetic and functional diversification of chemosensory signaling proteins in filarial nematode parasites, and encourage a more thorough investigation of clade and parasite-specific facets of nematode sensory receptor biology.

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Section: Discussionmentioning

confidence: 99%

Genetic and functional diversification of chemosensory pathway receptors in mosquito-borne filarial nematodes

Wheeler

Heimark

Airs

et al. 2019

Preprint

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“…Our and others’ results provide clues to understand how CNG channels with distinct subunit composition contribute to different cellular processes. Among CNG channels in C. elegans , TAX-2 and TAX-4 are essential for thermotaxis as well as for chemotaxis (Coburn and Bargmann, 1996; Komatsu et al, 1996), while CNG-3 seems to play a rather auxiliary role (O’Halloran et al, 2017). Although an α subunit TAX-4 can form a functional homo-tetramer that is far more sensitive to cGMP than the heteromer consisting of TAX-4 and a β subunit TAX-2 (Komatsu et al, 1999), TAX-2 that cannot form functional homomer by itself is still essential for thermosensation and chemosensation, indicating that heteromer-specific functions exist.…”

Section: Discussionmentioning

confidence: 99%

“…Although an α subunit TAX-4 can form a functional homo-tetramer that is far more sensitive to cGMP than the heteromer consisting of TAX-4 and a β subunit TAX-2 (Komatsu et al, 1999), TAX-2 that cannot form functional homomer by itself is still essential for thermosensation and chemosensation, indicating that heteromer-specific functions exist. CNG-3 was suggested to form a hetero-tetramer with TAX-4 and TAX-2 in AWC (O’Halloran et al, 2017), implying that a similar heteromer also forms in AFD. Considering our results suggesting that CNG-3 is necessary for steady state but not for transient state of thermotaxis, investigating how different composition of CNG channels function during such specific behavioral or cellular contexts in combination with analysis of their electrophysiological property would provide further understanding on roles of CNG channels in functions of the nervous system.…”

Section: Discussionmentioning

confidence: 99%

SLO potassium channels antagonize premature decision making in C. elegans

Aoki

Tateyama

Shimomura

et al. 2018

Preprint

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SummaryAnimals have to modify their behavior at the right timing to respond to changes in environments. Yet, the molecular and neural mechanisms regulating the timing of behavioral transition remain largely unknown. Performing forward genetics on a plasticity of thermotaxis behavior in C. elegans, we demonstrated that SLO potassium channels together with a cyclic nucleotide-gated channel CNG-3 determine the timing of the transition of temperature preference after shift of cultivation temperature. We further revealed that SLO and CNG-3 channels regulate the alteration in responsiveness of thermosensory neurons. Our results suggest that the regulation of sensory adaptation is a major determinant of the latency for animals to make decisions in changing behavior.HighlightsSlo-1 and SLO-2 K+ channels decelerated transition of temperature preference in thermotaxis behavior after upshift of cultivation temperatureSLO K+ channels slowed down the adaptation of AFD thermosensory neuron to new cultivation temperatureA cyclic nucleotide-gated channel CNG-3 functioned together with SLO-2Thermotaxis serves as could be a model system for early onset epilepsies

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“…Persistent odor stimulation in the absence of food results in a decreased attraction to the odor ( Bargmann, Hartwieg & Horvitz, 1993 ; Colbert & Bargmann, 1995 ; Ward, 1973 ). After 30 min of odor exposure to AWC-sensed odors, C. elegans displays a weak and transient decrease in attraction called short-term adaptation (henceforth called “adaptation”) that requires the cyclic nucleotide-gated channel subunit CNG-3 ( O’Halloran et al, 2017 ) and phosphorylation of the cyclic nucleotide-gated channel subunit TAX-2 by the cGMP-dependent protein kinase EGL-4 ( L’Etoile et al, 2002 ).…”

Section: Introductionmentioning

confidence: 99%

Odor-dependent temporal dynamics inCaenorhabitis elegansadaptation and aversive learning behavior

Choi

Lee

Kim

et al. 2018

PeerJ

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Animals sense an enormous number of cues in their environments, and, over time, can form learned associations and memories with some of these. The nervous system remarkably maintains the specificity of learning and memory to each of the cues. Here we asked whether the nematode Caenorhabditis elegans adjusts the temporal dynamics of adaptation and aversive learning depending on the specific odor sensed. C. elegans senses a multitude of odors, and adaptation and learned associations to many of these odors requires activity of the cGMP-dependent protein kinase EGL-4 in the AWC sensory neuron. We identified a panel of 17 attractive odors, some of which have not been tested before, and determined that the majority of these odors require the AWC primary sensory neuron for sensation. We then devised a novel assay to assess odor behavior over time for a single population of animals. We used this assay to evaluate the temporal dynamics of adaptation and aversive learning to 13 odors and find that behavior change occurs early in some odors and later in others. We then examined EGL-4 localization in early-trending and late-trending odors over time. We found that the timing of these behavior changes correlated with the timing of nuclear accumulation of EGL-4 in the AWC neuron suggesting that temporal changes in behavior may be mediated by aversive learning mechanisms. We demonstrate that temporal dynamics of adaptation and aversive learning in C. elegans can be used as a model to study the timing of memory formation to different sensory cues.

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Contribution of the cyclic nucleotide gated channel subunit, CNG-3, to olfactory plasticity in Caenorhabditis elegans

Cited by 23 publications

References 43 publications

Genetic and functional diversification of chemosensory pathway receptors in mosquito-borne filarial nematodes

Genetic and functional diversification of chemosensory pathway receptors in mosquito-borne filarial nematodes

SLO potassium channels antagonize premature decision making in C. elegans

Odor-dependent temporal dynamics inCaenorhabitis elegansadaptation and aversive learning behavior

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