Specific α- and β-Tubulin Isotypes Optimize the Functions of Sensory Cilia in<i>Caenorhabditis elegans</i>

Hurd, Daryl D.; Miller, Renee M.; Núñez, Lizbeth; Portman, Douglas S.

doi:10.1534/genetics.110.116996

Cited by 58 publications

(90 citation statements)

References 80 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The strains used in this study are as follows (Hurd et al, 2010). All strains used in this study carried the him-5(e1409) mutation, which generates a high incidence of males (Hodgkin et al, 1979).…”

Section: Strainsmentioning

confidence: 99%

“…In ray process ruptured males, 11 of 11 males could turn. Laser-mediated ablation of the ray A-neurons was undertaken in a strain carrying the transgene fsIs14 ( ptba-9::YFP ϩ ptba-6::mCherry ϩ psulp-3::GFP) (Hurd et al, 2010), which expresses YFP in the A-neurons and mCherry in the B-neurons. L4 males were isolated from the population and allowed to mature overnight.…”

Section: Laser-mediated Ray Cell Rupturing and Other Ablationsmentioning

confidence: 99%

“…The strains used in this study are as follows: trp-4(sy695)I (Li et al, 2006), cat-2 (e1112) II(Sulstonetal.,1975),tph-1(mg280) II(Szeetal.,2000), mab-5(e2088)III (Kenyon,1986),lin-39(n1872ts) III(Clarketal.,1993),unc-64(e246)III (Brenner, 1974), pha-1(e2123ts)III (Granato et al, 1994), pkd-2(sy606)IV (Barr et al, 2001), egl-3(ok979)V (Caenorhabditis Genetics Center), him-5(e1490) V, ceh-30(n4111n3714)X (Schwartz and Horvitz, 2007), lin-32(e1926)X (Zhao and Emmons, 1995), bxIs19 ( ptrp-4::GFP ϩ ttx-3::GFP), bxIs20 :nz ϩ pgrd-13::cz::Caspase-3 ϩ elt-2::GFP) (Barrios et al, 2008), nIs128 ( pkd-2::GFP) (Schwartz and Horvitz, 2007), mnIs12 (osm-6::GFP) (Collet et al, 1998), and fsIs14 ( ptba-9::YFP ϩ ptba-6::mCherry ϩ psulp-3::GFP) (Hurd et al, 2010). All strains used in this study carried the him-5(e1409) mutation, which generates a high incidence of males (Hodgkin et al, 1979).…”

Section: Strainsmentioning

confidence: 99%

“…The laser ablation method enabled us to eliminate a greater proportion of the A-neuron population. Laser ablations were performed in a strain carrying the transgenic array fsIs14, which expresses YFP in the A-neurons and mCherry in the B-neurons (Hurd et al, 2010). The use of this two-color system to distinguish A-versus B-neurons enabled us to verify that Aneuron ablation did not inadvertently cause collateral damage to the B-neurons, which are located in the same ganglia.…”

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

The Robustness ofCaenorhabditis elegansMale Mating Behavior Depends on the Distributed Properties of Ray Sensory Neurons and Their Output through Core and Male-Specific Targets

Koo

Bian²,

Sherlekar³

et al. 2011

J. Neurosci.

View full text Add to dashboard Cite

Many evolutionarily significant behaviors, such as mating, involve dynamic interactions with animate targets. This raises the question of what features of neural circuit design are essential to support these complex types of behavior. The Caenorhabditis elegans male uses 18 ray sensilla of the tail to coordinate mate apposition behavior, which facilitates a systematic search of the hermaphrodite surface for the vulva. Precisely how ray neuron types, A and B, robustly endow the male with a high degree of spatial and temporal precision is unknown. We show that the appositional postures that drive the search trajectory reflect the complex interplay of ray neuron type-induced motor outputs. Cell-type-specific ablations reveal that the A-neurons are required for all appositional postures. Their activity is instructive because the A-neurons can induce scanning-and turning-like appositional postures when artificially activated with channelrhodopsin (ChR2). B-neurons are essential only for initiation of the behavior in which they enhance male responsiveness to hermaphrodite contact. When artificially activated using ChR2, A-and B-neurons produce different tail ventral curl postures. However, when coactivated, A-neuron posture dominates, limiting B-neuron contributions to initiation or subsequent postures. Significantly, males lacking the majority of rays retain a high degree of postural control, indicating significant functional resilience in the system. Furthermore, eliminating a large number of male-specific ray neuron targets only partially attenuates tail posture control revealing that gender-common cells make an important contribution to the behavior. Thus, robustness may be a crucial feature of circuits underlying complex behaviors, such as mating, even in simple animals. IntroductionHow animals sense the relevant features of their environment and translate this information into appropriate motor responses is perhaps the overarching question in neuroscience. Ultimate and proximate mechanisms underlying mating success and the transmission of heritable information to the next generation is a central concern for evolutionary biology. The nematode worm Caenorhabditis elegans represents a valuable model system for exploring the molecular and cellular underpinnings of these two fundamental questions. Many studies of C. elegans behavior (for example, chemotaxis, thermotaxis, and mechanosensation) use hermaphrodites in simple behavioral assays (for review, see Bargmann, 2006;Goodman, 2006;Garrity et al., 2010). These behaviors are mediated by relatively few sensory receptor cells with limited in-built redundancy (Chalfie and Sulston, 1981;Bargmann and Horvitz, 1991;Biron et al., 2008). However, many evolutionarily significant behaviors involve dynamic interactions with animate targets. This raises the question of what features of neural circuit design are essential for supporting these more complex types of behavior. C. elegans male mating behavior consists of a carefully orchestrated sequence of sensorimotor transformati...

show abstract

Section: Strainsmentioning

confidence: 99%

Section: Laser-mediated Ray Cell Rupturing and Other Ablationsmentioning

confidence: 99%

Section: Strainsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

The Robustness ofCaenorhabditis elegansMale Mating Behavior Depends on the Distributed Properties of Ray Sensory Neurons and Their Output through Core and Male-Specific Targets

Koo

Bian²,

Sherlekar³

et al. 2011

J. Neurosci.

View full text Add to dashboard Cite

show abstract

“…The four male-specific CEM neurons are considered members of a single class based on substantial evidence: their fourfold symmetric location of cell bodies (14), the morphology of their processes (15), the morphology of their nuclei (16) and their cilia (17), and their gene expression (15,18,19). Presumptive CEMs die in the hermaphrodite (20) and are under coordinated genetic control, although the ventral CEMs are less sensitive to sexspecific apoptosis (16).…”

mentioning

confidence: 99%

Contrasting responses within a single neuron class enable sex-specific attraction in Caenorhabditis elegans

Narayan

Venkatachalam

Durak

et al. 2016

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

112

View full text Add to dashboard Cite

Animals find mates and food, and avoid predators, by navigating to regions within a favorable range of available sensory cues. How are these ranges set and recognized? Here we show that male Caenorhabditis elegans exhibit strong concentration preferences for sex-specific small molecule cues secreted by hermaphrodites, and that these preferences emerge from the collective dynamics of a single male-specific class of neurons, the cephalic sensory neurons (CEMs). Within a single worm, CEM responses are dissimilar, not determined by anatomical classification and can be excitatory or inhibitory. Response kinetics vary by concentration, suggesting a mechanism for establishing preferences. CEM responses are enhanced in the absence of synaptic transmission, and worms with only one intact CEM show nonpreferential attraction to all concentrations of ascaroside for which CEM is the primary sensor, suggesting that synaptic modulation of CEM responses is necessary for establishing preferences. A heterogeneous concentrationdependent sensory representation thus appears to allow a single neural class to set behavioral preferences and recognize ranges of sensory cues.T he chemical senses of taste and smell are an important source of sensory input for organisms from worms to humans, and elements of the olfactory system are evolutionarily conserved across metazoa (1, 2). The neural mechanisms of olfactory processing are a subject of active research (3), and much is known about the encoding of odor identity and concentration (4-6). However, the issue of ranges of favorable odor concentrations has been less studied. A reasonable general hypothesis is that physical sensory limitations set perceptual boundaries, limiting the range of an animal to respond favorably. However, there are instances where differences in odor concentrations can have different meanings: For example, both male and female rodents produce the same pheromone at different concentrations (7), and so males need to be able to distinguish between low and high concentrations. Similarly, a very high concentration might signal an adverse environment with overcrowding, in which case the animal is better off looking elsewhere. In such cases, the concentration preferences of the animals are tuned to some optimal value that has a higher probability of a successful outcome. Here, we show that Caenorhabditis elegans exhibits a striking tuning of pheromone concentration preferences, and that this concentration tuning is actively built and maintained by a single class of male-specific neurons, the cephalic sensory neurons (CEMs).The nervous system of C. elegans is famously compact, with 302 hermaphrodite neurons grouped into 118 classes based on morphology and connectivity (8), and 385 male neurons (9-11). Some classes of neurons are sex-specific (Fig. 1A). Members of a class are typically distinguished from each other by their relative anatomical position, such as left/right and dorsal/ventral. Although initially it was thought that members of a class were functionally similar, ...

show abstract

The tubulin code specializes neuronal cilia for extracellular vesicle release

Akella

Barr

2020

Developmental Neurobiology

View full text Add to dashboard Cite

Cilia are microtubule‐based organelles that display diversity in morphology, ultrastructure, protein composition, and function. The ciliary microtubules of C. elegans sensory neurons exemplify this diversity and provide a paradigm to understand mechanisms driving ciliary specialization. Only a subset of ciliated neurons in C. elegans are specialized to make and release bioactive extracellular vesicles (EVs) into the environment. The cilia of extracellular vesicle releasing neurons have distinct axonemal features and specialized intraflagellar transport that are important for releasing EVs. In this review, we discuss the role of the tubulin code in the specialization of microtubules in cilia of EV releasing neurons.

show abstract

Specific α- and β-Tubulin Isotypes Optimize the Functions of Sensory Cilia inCaenorhabditis elegans

Cited by 58 publications

References 80 publications

The Robustness ofCaenorhabditis elegansMale Mating Behavior Depends on the Distributed Properties of Ray Sensory Neurons and Their Output through Core and Male-Specific Targets

The Robustness ofCaenorhabditis elegansMale Mating Behavior Depends on the Distributed Properties of Ray Sensory Neurons and Their Output through Core and Male-Specific Targets

Contrasting responses within a single neuron class enable sex-specific attraction in Caenorhabditis elegans

The tubulin code specializes neuronal cilia for extracellular vesicle release

Contact Info

Product

Resources

About