The Wnt/ -Catenin Asymmetry Pathway Patterns the Atonal Ortholog lin-32 to Diversify Cell Fate in a Caenorhabditis elegans Sensory Lineage

Center for Neural Development and Disease, Department of Biomedical Genetics, University of Rochester School of Medicine and Dentistry, Rochester, New York 14642, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 09/2011; 31(37):13281-91. DOI: 10.1523/JNEUROSCI.6504-10.2011
Source: PubMed


Each sensory ray of the Caenorhabditis elegans male tail comprises three distinct neuroglial cell types. These three cells descend from a single progenitor, the ray precursor cell, through several rounds of asymmetric division called the ray sublineage. Ray development requires the conserved atonal-family bHLH gene lin-32, which specifies the ray neuroblast and promotes the differentiation of its progeny. However, the mechanisms that allocate specific cell fates among these progeny are unknown. Here we show that the distribution of LIN-32 during the ray sublineage is markedly asymmetric, localizing to anterior daughter cells in two successive cell divisions. The anterior-posterior patterning of LIN-32 expression and of differentiated ray neuroglial fates is brought about by the Wnt/β-catenin asymmetry pathway, including the Wnt ligand LIN-44, its receptor LIN-17, and downstream components LIT-1 (NLK), SYS-1 (β-catenin), and POP-1 (TCF). LIN-32 asymmetry itself has an important role in patterning ray cell fates, because the failure to silence lin-32 expression in posterior cells disrupts development of this branch of the ray sublineage. Together, our results illustrate a mechanism whereby the regulated function of a proneural-class gene in a single neural lineage can both specify a neural precursor and actively pattern the fates of its progeny. Moreover, they reveal a central role for the Wnt/β-catenin asymmetry pathway in patterning neural and glial fates in a simple sensory lineage.

Download full-text


Available from: Renee M Miller, Oct 01, 2015
19 Reads
  • [Show abstract] [Hide abstract]
    ABSTRACT: Proneural genes control the generation of neuroblasts from the neuroepithelium, but their functions in neuroblast asymmetric division and migration remain elusive. Here, we identified C. elegans mutants of a proneural transcription factor (TF) lin-32, in which Q neuroblasts are produced. We showed that LIN-32 functions in parallel with a storkhead TF, HAM-1, to regulate Q neuroblast asymmetric division, and that Q neuroblast migration is inhibited in lin-32 alleles. Consistently, lin-32 is expressed throughout Q neuroblast lineage, suggesting that LIN-32 may promote different target gene expression. Our studies thus uncovered previously unknown functions of a proneural gene in neuroblast development.
    FEBS letters 02/2014; 588(7). DOI:10.1016/j.febslet.2014.02.036 · 3.17 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: The vulva search corresponds to the first step of mating in C. elegans wherein the male recognizes a potential mate through contact and commences a systematic, contact-based search of her surface for the vulva. During this 'dance' the male presses his tail genitalia firmly against the hermaphrodite surface and moves backward, modulating tail posture to effect changes in search trajectory. Upon sensing the vulva, the male pauses and the insemination phase of mating begins. External tail sensilla, the rays, induce and guide the male's search by registering hermaphrodite surface cues. C. elegans male mating behavior, like many other animate interactions (such as predator-prey interactions or intrasexual aggression), is performed at close quarters and requires that participants constantly adjust their movement with respect to one another on a moment-by-moment basis. The design features of the supporting circuitry explain simultaneously the robustness, speed and acuity of the male's behavior and its male-specific nature. Processing at all levels of the circuitry appears to be distributed. Cellular components exhibit both partial redundancy (thus conferring robustness in output) and subtle functional differences (predicted to confer acuity). Surprisingly, gender-shared cell types feature prominently in the circuitry. Male-specific components form sensory pathways that render downstream gender-shared circuits responsive to mate cues, while other male cells act to augment gender-shared cell activity. Overall, the attributes of the vulva search circuitry provide insight into principles guiding the design and operation of circuits supporting dynamic social behaviors expressed by more complex and less tractable animal species.
    Seminars in Cell and Developmental Biology 05/2014; 33. DOI:10.1016/j.semcdb.2014.05.009 · 6.27 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The circuit structure and function underlying post-coital male behaviors remain poorly understood. Using mutant analysis, laser ablation, optogenetics, and Ca2+ imaging, we observed that following C. elegans male copulation, the duration of post-coital lethargy is coupled to cellular events involved in ejaculation. We show that the SPV and SPD spicule-associated sensory neurons and the spicule socket neuronal support cells function with intromission circuit components, including the cholinergic SPC and PCB and the glutamatergic PCA sensory-motor neurons, to coordinate sex muscle contractions with initiation and continuation of sperm movement. Our observations suggest that the SPV and SPD and their associated dopamine-containing socket cells sense the intrauterine environment through cellular endings exposed at the spicule tips and regulate both sperm release into the hermaphrodite and the recovery from post-coital lethargy. DOI:
    eLife Sciences 06/2014; 3(3):e02938. DOI:10.7554/eLife.02938 · 9.32 Impact Factor
Show more