Axial patterning of C. elegans male sensilla identities by selector genes

Lints, Robyn; Liu, Jia; Kim, K; Li, C; Emmons, Scott W.

doi:10.1016/j.ydbio.2004.01.021

Cited by 52 publications

(69 citation statements)

References 52 publications

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“…The concept can be applied to the level of individual cell types as well (for example, ref. 41). From this point of view, the cell-typespecific transcription factors cog-1, lin-11, and egl-38 can be thought of as selector genes for subsets of vulval cell types.…”

Section: Resultsmentioning

confidence: 99%

Transcriptional network underlying Caenorhabditis elegans vulval development

Inoué

Wang

Ririe

et al. 2005

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

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The vulval development of Caenorhabditis elegans provides an opportunity to investigate genetic networks that control gene expression during organogenesis. During the fourth larval stage (L4), seven vulval cell types are produced, each of which executes a distinct gene expression program. We analyze how the expression of cell-type-specific genes is regulated. Ras and Wnt signaling pathways play major roles in generating the spatial pattern of cell types and regulate gene expression through a network of transcription factors. One transcription factor (lin-29) primarily controls the temporal expression pattern. Other transcription factors (lin-11, cog-1, and egl-38) act in combination to control cell-typespecific gene expression. The complexity of the network arises in part because of the dynamic nature of gene expression, in part because of the presence of seven cell types, and also because there are multiple regulatory paths for gene expression within each cell type.organogenesis ͉ signaling pathways ͉ transcription D evelopmental events are driven by spatially and temporally regulated gene expression. Understanding how complex patterns of expression are produced is therefore a critical part of deciphering mechanisms of development. In general, intercellular signaling mechanisms interact with a network of transcription factors to generate cell-type-specific patterns of gene expression. The late stage of Caenorhabditis elegans vulval development offers a useful model in which to study this process. During this period of vulval development, seven distinct cell types are produced that express unique combinations of genes. Over the last several years, a number of genes were discovered that are expressed in cell-type and stage-specific patterns in the vulva, and several transcription factors were found to regulate these genes. In this paper, we synthesize and extend our current knowledge of this genetic network.The C. elegans vulva connects the uterine lumen to the outside, allowing for passage of sperm and fertilized eggs (1). Vulval cells are generated postembryonically from precursor cells P3.p P4.p, P5.p, P6.p, P7.p, and P8.p [also called vulval precursor cells (VPC)]. During the mid-third larval (L3) stage, EGF and Notch signaling induces the middle three VPCs (P5.p, P6.p, and P7.p) to adopt vulval fates, whereas P3.p, P4.p, and P8.p fuse with the hypodermal syncytium, hyp7 (2-6).During the late-L3 to the early-L4 stage, P5.p, P6.p, and P7.p undergo two or three rounds of cell division to produce 22 nuclei (7) (Fig. 1A). These nuclei are in cells of seven types (vulA, vulB1, vulB2, vulC, vulD, vulE, and vulF), as evidenced by subsequent morphogenetic movements and by the pattern of gene expression (8, 9) (Fig. 1B). The seven cell types that are present in the adult vulva represent specializations within the general epithelial cell class. These cells exhibit cell-type general features; for example, each expresses ajm-1, a component of the apical junction that connects neighboring cells in epithelial tissues (8)....

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Section: Resultsmentioning

confidence: 99%

Transcriptional network underlying Caenorhabditis elegans vulval development

Inoué

Wang

Ririe

et al. 2005

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

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“…As described above, the orientation of ray openings alternate along the A-P axis, and ray pairs have a characteristic shape (Sulston and Horvitz, 1977;Sulston et al, 1980). Furthermore, A-and B-type neuron populations can be divided into subtypes based on neurotransmitter fate, and these fates are not exclusively paired with a given ray morphology (Sulston and Horvitz, 1977;Lints et al, 2004). These various features could confer functional specialization among different ray pairs.…”

Section: Introductionmentioning

confidence: 98%

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.

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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...

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“…In addition to dopamine and serotonin, C. elegans contains a complex profile of FMRFamide-like (FaRP) neuropeptide in RnB neurons (4). We found that the specification of FaRP neuronal fate is also affected in sor-3 and sop-2 mutants.…”

Section: Resultsmentioning

confidence: 85%

“…Each finger-like sensory ray consists of the dendritic endings of two distinct neurons, an A-type neuron (RnA) and a B-type neuron (RnB), wrapped in the process of a glial-like structural cell (Rnst) (where n stands for rays [1][2][3][4][5][6][7][8][9]. A subset of A-type neurons, R5A, R7A, and R9A, express the neurotransmitter dopamine, whereas a subset of B-type neurons, R1B, R3B, and R9B, express serotonin.…”

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confidence: 99%

“…A subset of A-type neurons, R5A, R7A, and R9A, express the neurotransmitter dopamine, whereas a subset of B-type neurons, R1B, R3B, and R9B, express serotonin. Previous studies show that a TGF-␤ signaling pathway and Hox gene egl-5 (ortholog of Drosophila Abd-B) play important roles in the specification of dopaminergic and serotonergic ray neurons (3,4). The identification of additional genes involved in specifying neurotransmitter phenotype may contribute to our understanding of the molecular mechanisms underlying the formation of neurons with defined neurotransmitters in other organisms.…”

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confidence: 99%

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Polycomb -like genes are necessary for specification of dopaminergic and serotonergic neurons in Caenorhabditis elegans

Yang

Sun

Luo

et al. 2007

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

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The molecular mechanisms underlying the formation of neurons with defined neurotransmitters are not well understood. In this study, we demonstrate that the PcG-like genes in Caenorhabditis elegans, sop-2 and sor-3, regulate the formation of dopaminergic and serotonergic neurons and several other neuronal properties. sor-3 encodes a novel protein containing an MBT repeat, a domain that contains histone-binding activity and is present in PcG proteins SCM and Sfmbt in other organisms. We further show that mutations in sor-3 lead to ectopic expression of Hox genes and cause homeotic transformations. Specification of certain neuronal identities by these PcG-like genes appears to involve regulation of non-Hox gene targets. Our studies revealed that the PcG-like genes are crucial for coordinately regulating the expression of discrete aspects of neuronal identities in C. elegans.Hox genes ͉ PcG ͉ sop-2 ͉ sor-3

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Axial patterning of C. elegans male sensilla identities by selector genes

Cited by 52 publications

References 52 publications

Transcriptional network underlying Caenorhabditis elegans vulval development

Transcriptional network underlying Caenorhabditis elegans vulval development

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

Polycomb -like genes are necessary for specification of dopaminergic and serotonergic neurons in Caenorhabditis elegans

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