Transmembrane protein MIG-13 links the Wnt signaling and Hox genes to the cell polarity in neuronal migration

Wang, Xiangming; Zhou, Fanli; Lv, Sijing; Yi, Peishan; Zhu, Zhiwen; Yang, Yihong; Feng, Guoying; Li, Wei; Ou, Guangshuo

doi:10.1073/pnas.1301849110

Cited by 42 publications

(72 citation statements)

References 30 publications

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“…MAB-5 is required in QL to direct QL descendant migrations including PQR (Salser and Kenyon 1992) (Figure 1, A and E). LIN-39 has been shown to cell-autonomously promote anterior migration of QR descendants, and lin-39 is normally inhibited by MAB-5 in QL.a/p to allow for posterior migration (Figure 1, A and F) (Harris et al 1996;Wang et al 2013).…”

Section: Resultsmentioning

confidence: 99%

“…mab-5 is not expressed in QR descendants (Salser et al 1993;Harris et al 1996;Salser and Kenyon 1996), and lin-39 autonomously drives anterior QR descendant migration and is repressed in QL by mab-5 (Harris et al 1996;Wang et al 2013). However, both are expressed in other posterior cells, including P cells, and MAB-5 in posterior BWMs and seam cells (Salser et al 1993;Wang et al 1993;Clandinin et al 1997;Maloof et al 1999;Yang et al 2005;Wagmaister et al 2006a,b) (Figure 1C).…”

Section: Resultsmentioning

confidence: 99%

“…Both QL and QR initially express lin-39, but mab-5 inhibits lin-39 expression in QL when it is expressed in response to Wnt signaling (Clark et al 1993;Salser et al 1993;Wang et al 2013). lin-39 drives expression of the MIG-13 transmembrane receptor molecule in QL descendants, which, along with SDN-1/syndecan, mediates anterior migration (Wang et al 2013;Sundararajan et al 2015).…”

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confidence: 99%

“…Next, mab-5 is expressed in QL, but also in posterior body wall muscles (BWMs), P7-P12, and the V5 and V6 hypodermal seam cells (Kenyon 1986;Salser and Kenyon 1996;Ji et al 2013). MAB-5 and LIN-39 can act in parallel in the P cells, where they are both expressed, or play opposing roles in Q neuroblast migration where MAB-5 directs posterior migration, and LIN-39 promotes anterior migration (Salser and Kenyon 1992;Clark et al 1993;Wang et al 2013). MAB-5 also interacts genetically with the more posteriorly expressed Hox gene egl-5 (Chisholm 1991;Ferreira et al 1999).…”

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confidence: 99%

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Nonautonomous Roles of MAB-5/Hox and the Secreted Basement Membrane Molecule SPON-1/F-Spondin in Caenorhabditis elegans Neuronal Migration

2016

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Nervous system development and circuit formation requires neurons to migrate from their birthplaces to specific destinations.Migrating neurons detect extracellular cues that provide guidance information. In Caenorhabditis elegans, the Q right (QR) and Q left (QL) neuroblast descendants migrate long distances in opposite directions. The Hox gene lin-39 cell autonomously promotes anterior QR descendant migration, and mab-5/Hox cell autonomously promotes posterior QL descendant migration. Here we describe a nonautonomous role of mab-5 in regulating both QR and QL descendant migrations, a role masked by redundancy with lin-39. A third Hox gene, egl-5/Abdominal-B, also likely nonautonomously regulates Q descendant migrations. In the lin-39 mab-5 egl-5 triple mutant, little if any QR and QL descendant migration occurs. In addition to well-described roles of lin-39 and mab-5 in the Q descendants, our results suggest that lin-39, mab-5, and egl-5 might also pattern the posterior region of the animal for Q descendant migration. Previous studies showed that the spon-1 gene might be a target of MAB-5 in Q descendant migration. spon-1 encodes a secreted basement membrane molecule similar to vertebrate F-spondin. Here we show that spon-1 acts nonautonomously to control Q descendant migration, and might function as a permissive rather than instructive signal for cell migration. We find that increased levels of MAB-5 in body wall muscle (BWM) can drive the spon-1 promoter adjacent to the Q cells, and loss of spon-1 suppresses mab-5 gain of function. Thus, MAB-5 might nonautonomously control Q descendant migrations by patterning the posterior region of the animal to which Q cells respond. spon-1 expression from BWMs might be part of the posterior patterning necessary for directed Q descendant migration.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Nonautonomous Roles of MAB-5/Hox and the Secreted Basement Membrane Molecule SPON-1/F-Spondin in Caenorhabditis elegans Neuronal Migration

2016

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“…It appears that neuronal differentiation is more sensitive to the failures of asymmetric cell division and apoptosis than the defect of neuronal migration. For example, a single transmembrane protein MIG-13 specifically regulates the anterior migration of QR neuroblast descendants [9]; and the AQR and AVM fail to reach their correct positions in mig-13 mutants but they appear to properly differentiate by examining the Pmec-4::gfp reporter (N>1,000).…”

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The role of apoptosis in Caenorhabditis elegans neuronal differentiation

Tian

Zhu

et al. 2015

Sci. China Life Sci.

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Dear Editor, Neuronal apoptosis is considered to be essential for brain development and neurodegenerative disorders and has been a major focus in cell biological and neuroscientific studies since its first recognition a century ago [1]. Remarkable progress has been made in defining the molecular and cellular pathways underlying neuronal apoptosis during the past decade [2], however, it remains relatively unclear about the physiological functions of apoptosis in neural development. The neurotrophin hypothesis proposes that immature neurons compete for trophic factors that are derived from target neurons in limited supply and that only neurons that successfully establish synaptic connections with their targets would receive trophic support to survive [3]. Although this model is appealing in predicting neuronal survival, it does not explain how to trigger neuronal apoptosis in the absence of trophic factors. Moreover, the neurotrophin hypothesis may not apply to the model organism such as Caenorhabditis elegans in which the canonic nerve growth factors have not been reported yet.Alternative models can be valuable to illustrate the physiological function of neuronal apoptosis. Among the 1,090 somatic cells generated during the development of the C. elegans hermaphrodite, 131 cells undergo programmed cell death [4]; and 105 of the 131 apoptotic cells are derived from neuronal cell lineages. Intriguingly, many neuronal apoptotic events in C. elegans are coupled with asymmetric cell divisions (ACDs): neuroblast asymmetric division produces a small daughter cell that undergoes apoptosis and a large daughter cell that differentiates or divides and differentiates into neurons ( Figure 1A for Q neuroblast lineages). The recent finding about the segregation of aggresomes during asymmetric divisions suggests another possible model for the function of neuronal apoptosis [5]. Perhaps in C. elegans neuroblast lineages, misfolded proteins asymmetrically segregate to the daughter cell that is destined to die. Similarly, factors that may inhibit neuronal differentiation may be asymmetrically inherited by the apoptotic daughter cell for degradation. The "asymmetric segregation" model would assume that neuronal apoptosis removes misfolded protein or differentiation inhibitors, maintaining the fitness of neurons or promoting neuronal differentiation. This model can be examined by inhibiting neuroblast cytokinesis: if aggresomes or differentiation inhibitors could not be segregated, the defects of neuronal differentiation or function should be expected in adult nematodes. However, this model was previously difficult to be tested because of the lack of genetic tools to manipulate neuroblast cytokinesis in live animals.To provide some tangible evidence for the "asymmetric segregation" hypothesis, we here applied two approaches to generate conditional mutations or a weak mutant allele that disrupts neuroblast cytokinesis but allows animal to survive ( Figure 1B). We chose to target an evolutionarily conserved cytokinetic scaffold protein...

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The Caenorhabditis elegans Q neuroblasts: A powerful system to study cell migration at single‐cell resolution in vivo

Rella

Póvoa

Korswagen

2016

Genesis

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Summary: During development, cell migration plays a central role in the formation of tissues and organs. Understanding the molecular mechanisms that drive and control these migrations is a key challenge in developmental biology that will provide important insights into disease processes, including cancer cell metastasis. In this article, we discuss the Caenorhabditis elegans Q neuroblasts and their descendants as a tool to study cell migration at single-cell resolution in vivo. The highly stereotypical migration of these cells provides a powerful system to study the dynamic cytoskeletal processes that drive migration as well as the evolutionarily conserved signaling pathways (including different Wnt signaling cascades) that guide the cells along their specific trajectories. Here, we provide an overview of what is currently known about Q neuroblast migration and highlight the live-cell imaging, genome editing, and quantitative gene expression techniques that have been developed to study this process. genesis 54:198-211,

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Transmembrane protein MIG-13 links the Wnt signaling and Hox genes to the cell polarity in neuronal migration

Cited by 42 publications

References 30 publications

Nonautonomous Roles of MAB-5/Hox and the Secreted Basement Membrane Molecule SPON-1/F-Spondin in Caenorhabditis elegans Neuronal Migration

Nonautonomous Roles of MAB-5/Hox and the Secreted Basement Membrane Molecule SPON-1/F-Spondin in Caenorhabditis elegans Neuronal Migration

The role of apoptosis in Caenorhabditis elegans neuronal differentiation

The Caenorhabditis elegans Q neuroblasts: A powerful system to study cell migration at single‐cell resolution in vivo

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