Lineage, cell polarity and inscuteable function in the peripheral nervous system of the Drosophila embryo

Development ◽  
2001 ◽  
Vol 128 (5) ◽  
pp. 631-643 ◽  
Author(s):  
V. Orgogozo ◽  
F. Schweisguth ◽  
Y. Bellaiche

The stereotyped pattern of the Drosophila embryonic peripheral nervous system (PNS) makes it an ideal system to use to identify mutations affecting cell polarity during asymmetric cell division. However, the characterisation of such mutations requires a detailed description of the polarity of the asymmetric divisions in the sensory organ lineages. We describe the pattern of cell divisions generating the vp1-vp4a mono-innervated external sense (es) organs. Each sensory organ precursor (SOP) cell follows a series of four asymmetric cell divisions that generate the four es organs cells (the socket, shaft, sheath cells and the es neurone) together with one multidendritic (md) neurone. This lineage is distinct from any of the previously proposed es lineages. Strikingly, the stereotyped pattern of cell divisions in this lineage is identical to those described for the embryonic chordotonal organ lineage and for the adult thoracic bristle lineage. Our analysis reveals that the vp2-vp4a SOP cells divide with a planar polarity to generate a dorsal pIIa cell and a ventral pIIb cell. The pIIb cell next divides with an apical-basal polarity to generate a basal daughter cell that differentiates as an md neurone. We found that Inscuteable specifically accumulated at the apical pole of the dividing pIIb cell and regulated the polarity of the pIIb division. This study establishes for the first time the function of Inscuteable in the PNS, and provides the basis for studying the mechanisms controlling planar and apical-basal cell polarities in the embryonic sensory organ lineages.

Genetics ◽  
2000 ◽  
Vol 155 (2) ◽  
pp. 733-752 ◽  
Author(s):  
Salim Abdelilah-Seyfried ◽  
Yee-Ming Chan ◽  
Chaoyang Zeng ◽  
Nicholas J Justice ◽  
Susan Younger-Shepherd ◽  
...  

Abstract The Drosophila adult external sensory organ, comprising a neuron and its support cells, is derived from a single precursor cell via several asymmetric cell divisions. To identify molecules involved in sensory organ development, we conducted a tissue-specific gain-of-function screen. We screened 2293 independent P-element lines established by P. Rørth and identified 105 lines, carrying insertions at 78 distinct loci, that produced misexpression phenotypes with changes in number, fate, or morphology of cells of the adult external sensory organ. On the basis of the gain-of-function phenotypes of both internal and external support cells, we subdivided the candidate lines into three classes. The first class (52 lines, 40 loci) exhibits partial or complete loss of adult external sensory organs. The second class (38 lines, 28 loci) is associated with increased numbers of entire adult external sensory organs or subsets of sensory organ cells. The third class (15 lines, 10 loci) results in potential cell fate transformations. Genetic and molecular characterization of these candidate lines reveals that some loci identified in this screen correspond to genes known to function in the formation of the peripheral nervous system, such as big brain, extra macrochaetae, and numb. Also emerging from the screen are a large group of previously uncharacterized genes and several known genes that have not yet been implicated in the development of the peripheral nervous system.


Development ◽  
2000 ◽  
Vol 127 (17) ◽  
pp. 3735-3743 ◽  
Author(s):  
V. Van De Bor ◽  
R. Walther ◽  
A. Giangrande

In flies, the choice between neuronal and glial fates depends on the asymmetric division of multipotent precursors, the neuroglioblast of the central nervous system and the IIb precursor of the sensory organ lineage. In the central nervous system, the choice between the two fates requires asymmetric distribution of the glial cell deficient/glial cell missing (glide/gcm) RNA in the neuroglioblast. Preferential accumulation of the transcript in one of the daughter cells results in the activation of the glial fate in that cell, which becomes a glial precursor. Here we show that glide/gcm is necessary to induce glial differentiation in the peripheral nervous system. We also present evidence that glide/gcm RNA is not necessary to induce the fate choice in the peripheral multipotent precursor. Indeed, glide/gcm RNA and protein are first detected in one daughter of IIb but not in IIb itself. Thus, glide/gcm is required in both central and peripheral glial cells, but its regulation is context dependent. Strikingly, we have found that only subsets of sensory organs are gliogenic and express glide/gcm. The ability to produce glial cells depends on fixed, lineage related, cues and not on stochastic decisions. Finally, we show that after glide/gcm expression has ceased, the IIb daughter migrates and divides symmetrically to produce several mature glial cells. Thus, the glide/gcm-expressing cell, also called the fifth cell of the sensory organ, is indeed a glial precursor. This is the first reported case of symmetric division in the sensory organ lineage. These data indicate that the organization of the fly peripheral nervous system is more complex than previously thought.


2019 ◽  
Author(s):  
Matthew H. Rowe ◽  
Juan Dong ◽  
Annika K. Weimer ◽  
Dominique C. Bergmann

SUMMARYGenerating cell polarity in anticipation of asymmetric cell division is required in many developmental contexts across a diverse range of species. Physical and genetic diversity among major multicellular taxa, however, demand different molecular solutions to this problem. The Arabidopsis stomatal lineage displays asymmetric, stem cell-like and oriented cell divisions, which require the activity of the polarly localized protein, BASL. Here we identify the plant-specific BREVIS RADIX (BRX) family as localization and activity partners of BASL. We show that members of the BRX family are polarly localized to peripheral domains in stomatal lineage cells and that their collective activity is required for asymmetric cell divisions. We further demonstrate a mechanism for these behaviors by uncovering mutual, yet unequal dependencies of BASL and the BRX family for each other’s localization and segregation at the periphery of stomatal lineage cells.


2019 ◽  
Author(s):  
Suzanne E. M. van der Horst ◽  
Janine Cravo ◽  
Alison Woollard ◽  
Juliane Teapal ◽  
Sander van den Heuvel

ABSTRACTA correct balance between proliferative and asymmetric cell divisions underlies normal development, stem cell maintenance and tissue homeostasis. What determines whether cells undergo symmetric or asymmetric cell division is poorly understood. To gain insight in the mechanisms involved, we studied the stem cell-like seam cells in the Caenorhabditis elegans epidermis. Seam cells go through a reproducible pattern of asymmetric divisions, instructed by non-canonical Wnt/β-catenin asymmetry signaling, and symmetric divisions that increase the seam cell number. Using time-lapse fluorescence microscopy, we show that symmetric cell divisions maintain the asymmetric localization of Wnt/β-catenin pathway components. Observations based on lineage-specific knockout and GFP-tagging of endogenous pop-1 support the model that POP-1TCF induces differentiation at a high nuclear level, while low nuclear POP-1 promotes seam cell self-renewal. Before symmetric division, the transcriptional regulator rnt-1Runx and cofactor bro-1CBFβ temporarily bypass Wnt/β-catenin asymmetry by downregulating pop-1 expression. Thereby, RNT-1/BRO-1 appears to render POP-1 below the level required for its repressor function, which converts differentiation into self-renewal. Thus, opposition between the C. elegans Runx/CBFβ and TCF stem-cell regulators controls the switch between asymmetric and symmetric seam cell division.


Cell ◽  
1993 ◽  
Vol 73 (7) ◽  
pp. 1307-1321 ◽  
Author(s):  
Andrew P. Jarman ◽  
Yves Grau ◽  
Lily Y. Jan ◽  
Yuh Nung Jan

2020 ◽  
Author(s):  
Yan Gong ◽  
Julien Alassimone ◽  
Rachel Varnau ◽  
Nidhi Sharma ◽  
Lily S. Cheung ◽  
...  

ABSTRACTAsymmetric and self-renewing divisions build and pattern tissues. In the Arabidopsis thaliana stomatal lineage, asymmetric cell divisions, guided by polarly localized cortical proteins, generate the majority of cells on the leaf surface. These divisions can be fine-tuned by systemic and environmental signals to modify tissue development, but the molecular mechanisms by which plants incorporate such cues to regulate asymmetric divisions are largely unknown. In a screen for modulators of cell polarity and asymmetric divisions, we identified a mutation in CONSTITIUTIVE TRIPLE RESPONSE 1, a negative regulator of ethylene signaling. We subsequently revealed antagonistic impacts of ethylene and glucose signaling on the self-renewing capacity of stomatal lineage stem cells. Quantitative analysis of the impacts of these signaling systems on cell polarity and fate dynamics showed that developmental information may be encoded in both the spatial and temporal asymmetries of polarity proteins. Taken together, our results provide a framework for a mechanistic understanding of how systemic information such as nutritional status and environmental factors tune stem cell behavior in the stomatal lineage, ultimately enabling optimization of leaf size and cell-type composition.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Yan Gong ◽  
Julien Alassimone ◽  
Rachel Varnau ◽  
Nidhi Sharma ◽  
Lily S Cheung ◽  
...  

Asymmetric and self-renewing divisions build and pattern tissues. In the Arabidopsis stomatal lineage, asymmetric cell divisions, guided by polarly localized cortical proteins, generate most cells on the leaf surface. Systemic and environmental signals modify tissue development, but the mechanisms by which plants incorporate such cues to regulate asymmetric divisions are elusive. In a screen for modulators of cell polarity, we identified CONSTITUTIVE TRIPLE RESPONSE1, a negative regulator of ethylene signaling. We subsequently revealed antagonistic impacts of ethylene and glucose signaling on the self-renewing capacity of stomatal lineage stem cells. Quantitative analysis of cell polarity and fate dynamics showed that developmental information may be encoded in both the spatial and temporal asymmetries of polarity proteins. These results provide a framework for a mechanistic understanding of how nutritional status and environmental factors tune stem-cell behavior in the stomatal lineage, ultimately enabling flexibility in leaf size and cell-type composition.


2021 ◽  
Author(s):  
Pil Jung Kang ◽  
Rachel Mullner ◽  
Haoyu Li ◽  
Derek Hansford ◽  
Han-Wei Shen ◽  
...  

ABSTRACTCell polarity underlies various cellular processes, including cell proliferation and asymmetric cell division. Cdc42, a conserved Rho GTPase, plays a central role in polarity establishment in yeast and animals. While cell polarity is critical for the asymmetric division of budding yeast, whether Cdc42 impacts lifespan is not clear. Here, we show by live-cell imaging that the active Cdc42 level is sporadically elevated in wild-type cells during repeated cell divisions but rarely in the long-lived bud8 deletion mutant. Remarkably, mild overexpression of Cdc42 causes premature aging with frequent symmetric cell divisions despite no harmful effects on young cells. Furthermore, deletion of BUD8 rescues the short lifespan of an rga1 mutant, which lacks a Cdc42 GTPase activating protein, and Bud8 competes with Rga1 for localization to cytokinesis remnants. Collectively, our findings suggest that upregulation of Cdc42 is a proximal cause of cell death in old yeast cells and that Bud8 counteracts Rga1 in modulating the Cdc42 activity to limit replicative lifespan.


Author(s):  
S.S. Spicer ◽  
B.A. Schulte

Generation of monoclonal antibodies (MAbs) against tissue antigens has yielded several (VC1.1, HNK- 1, L2, 4F4 and anti-leu 7) which recognize the unique sugar epitope, glucuronyl 3-sulfate (Glc A3- SO4). In the central nervous system, these MAbs have demonstrated Glc A3-SO4 at the surface of neurons in the cerebral cortex, the cerebellum, the retina and other widespread regions of the brain.Here we describe the distribution of Glc A3-SO4 in the peripheral nervous system as determined by immunostaining with a MAb (VC 1.1) developed against antigen in the cat visual cortex. Outside the central nervous system, immunoreactivity was observed only in peripheral terminals of selected sensory nerves conducting transduction signals for touch, hearing, balance and taste. On the glassy membrane of the sinus hair in murine nasal skin, just deep to the ringwurt, VC 1.1 delineated an intensely stained, plaque-like area (Fig. 1). This previously unrecognized structure of the nasal vibrissae presumably serves as a tactile end organ and to our knowledge is not demonstrable by means other than its selective immunopositivity with VC1.1 and its appearance as a densely fibrillar area in H&E stained sections.


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