Functional transcriptomic analysis of the role of MAB-5/Hox in Q neuroblast migration in Caenorhabditis elegans

Tamayo, Joel V.; Gujar, Mahekta R; Macdonald, Stuart J.; Lundquist, Erik A.

doi:10.1186/1471-2164-14-304

Cited by 19 publications

(42 citation statements)

References 51 publications

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“…Potential MAB-5 transcriptional targets in Q descendant migration were identified previously by whole-animal RNA-seq on wild-type and mab-5 mutants coupled with functional suppression of mab-5(e1751) gof (Tamayo et al 2013). spon-1 transcripts were over-represented in mab-5(gof), and reduction of spon-1 function partially suppressed posterior AQR migration in mab-5(gof) (Tamayo et al 2013).…”

Section: Spon-1 Is Required For Proper Q Descendant Migrationmentioning

confidence: 71%

“…spon-1 transcripts were over-represented in mab-5(gof), and reduction of spon-1 function partially suppressed posterior AQR migration in mab-5(gof) (Tamayo et al 2013). These results indicate that spon-1 expression is regulated by MAB-5 and that SPON-1 is required for posterior AQR migration in mab-5(gof).…”

Section: Spon-1 Is Required For Proper Q Descendant Migrationmentioning

confidence: 77%

“…The genes that MAB-5 controls to drive posterior migration are largely unknown. A recent study used whole organism RNA sequencing (RNA-seq) of mab-5 mutants paired with functional analysis to determine genes regulated by MAB-5 in migration (Tamayo et al 2013). This study found enrichment for secreted and transmembrane molecules regulated by MAB-5, suggesting that MAB-5 might directly regulate a cell's interaction with its environment.…”

mentioning

confidence: 99%

“…A previous RNA-seq study identified spon-1 as a potential transcriptional target of MAB-5 (Tamayo et al 2013). The mab-5(e1751) gain-of-function (gof) mutation causes ectopic expression of mab-5 in many cells, including QR, and drives posterior migration of the QR descendant AQR (Salser et al 1993;Chapman et al 2008).…”

mentioning

confidence: 99%

“…The mab-5(e1751) gain-of-function (gof) mutation causes ectopic expression of mab-5 in many cells, including QR, and drives posterior migration of the QR descendant AQR (Salser et al 1993;Chapman et al 2008). RNA-mediated interference (RNAi) knockdown of spon-1 partially suppressed posterior AQR migration in mab-5(gof), suggesting that spon-1 mediates the effects of mab-5(gof) in posterior migration (Tamayo et al 2013). spon-1 encodes a secreted basement membrane molecule similar to vertebrate F-spondin (Woo et al 2008).…”

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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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: Spon-1 Is Required For Proper Q Descendant Migrationmentioning

confidence: 71%

Section: Spon-1 Is Required For Proper Q Descendant Migrationmentioning

confidence: 77%

mentioning

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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The MAB-5/Hox family transcription factor is important for Caenorhabditis elegans innate immune response to Staphylococcus epidermidis infection

Kywe,

Lundquist,

Ackley

et al. 2024

G3: Genes, Genomes, Genetics

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Innate immunity functions as a rapid defense against broad classes of pathogenic agents. While the mechanisms of innate immunity in response to antigen exposure are well-studied, how pathogen exposure activates the innate immune responses and the role of genetic variation in immune activity is currently being investigated. Previously we showed significant survival differences between the N2 and CB4856 Caenorhabditis elegans isolates in response to Staphylococcus epidermidis infection. One of those differences was expression of the mab-5 Hox-family transcription factor, which was induced in N2, but not CB4856, after infection. Here we use survival assays and RNA-sequencing to better understand the role of mab-5 in response to S. epidermidis. We found that mab-5 loss-of-function mutants were more susceptible to S. epidermidis infection than N2 or mab-5 gain-of-function mutants, but not as susceptible as CB4856 animals. We then conducted transcriptome analysis of infected worms and found considerable differences in gene-expression profiles when comparing animals with mab-5 loss-of-function to either N2 or mab-5 gain-of-function. N2 and mab-5 gain-of-function animals showed a significant enrichment in expression of immune genes and C-type lectins, whereas mab-5 loss-of-function mutants did not. Overall, gene expression profiling in mab-5 mutants provided insight into MAB-5 regulation of the transcriptomic response of C. elegans to pathogenic bacteria and helps us to understand mechanisms of innate immune activation and the role that transcriptional regulation plays in organismal health.

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MAB-5/Hox regulates the Q neuroblast transcriptome, including cwn-1/Wnt, to mediate posterior migration in Caenorhabditis elegans

Paolillo,

Ochs,

Lundquist

2024

Genetics

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Neurogenesis involves the precisely coordinated action of genetic programs controlling large-scale neuronal fate specification down to terminal events of neuronal differentiation. The Q neuroblasts in Caenorhabditis elegans, QL on the left and QR on the right, divide, differentiate, and migrate in a similar pattern to produce three neurons each. However, QL on the left migrates posteriorly, and QR on the right migrates anteriorly. The MAB-5/Hox transcription factor is necessary and sufficient for posterior Q lineage migration and is normally expressed only in the QL lineage. To define genes controlled by MAB-5 in the Q cells, fluorescence-activated cell sorting was utilized to isolate populations of Q cells at a time in early L1 larvae when MAB-5 first becomes active. Sorted Q cells from wild-type, mab-5 loss-of-function (lof), and mab-5 gain-of-function (gof) mutants were subject to RNA-seq and differential expression analysis. Genes enriched in Q cells included those involved in cell division, DNA replication, and DNA repair, consist with the neuroblast stem cell identity of the Q cells at this stage. Genes affected by mab-5 included those involved in neurogenesis, neural development, and interaction with the extracellular matrix. cwn-1, which encodes a Wnt signaling molecule, showed a paired response to mab-5 in the Q cells: cwn-1 expression was reduced in mab-5(lof) and increased in mab-5(gof), suggesting that MAB-5 is required for cwn-1 expression in Q cells. MAB-5 is required to prevent anterior migration of the Q lineage while it transcriptionally reprograms the Q lineage for posterior migration. Functional genetic analysis revealed that CWN-1 is required downstream of MAB-5 to inhibit anterior migration of the QL lineage, likely in parallel to EGL-20/Wnt in a noncanonical Wnt pathway. In sum, work here describes a Q cell transcriptome, and a set of genes regulated by MAB-5 in the QL lineage. One of these genes, cwn-1, acts downstream of mab-5 in QL migration, indicating that this gene set includes other genes utilized by MAB-5 to facilitate posterior neuroblast migration.

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Functional transcriptomic analysis of the role of MAB-5/Hox in Q neuroblast migration in Caenorhabditis elegans

Cited by 19 publications

References 51 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 MAB-5/Hox family transcription factor is important for Caenorhabditis elegans innate immune response to Staphylococcus epidermidis infection

MAB-5/Hox regulates the Q neuroblast transcriptome, including cwn-1/Wnt, to mediate posterior migration in Caenorhabditis elegans

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