The transcriptional regulator lola is required for stem cell maintenance and germ cell differentiation in the Drosophila testis

Davies, Erin L.; Lim, Jaclyn; Joo, William; Tam, Cheuk Ho; Fuller, Margaret T.

doi:10.1016/j.ydbio.2012.11.004

Cited by 26 publications

(31 citation statements)

References 40 publications

(58 reference statements)

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“…Therefore, three relatively well-studied Lola proteins (LolaA, LolaL, and LolaT) were tested for the physical association with PKG by coimmunoprecipitation experiments using Drosophila S2 cells. However, the three Lola isoforms in our study are in accordance with those in Flybase by reason of different naming conventions (Davies et al, 2013). Flag-tagged PKG (Flag-PKG-P2) and each of the three different Myc-tagged Lola isoforms (Myc-LolaA, Myc-LolaL, Myc-LolaT) were cooverexpressed in S2 cells.…”

Section: Pkg Physically Interacts With Lolat Both In Vitro and In Vivosupporting

confidence: 58%

“…PKG is an important intracellular effector of the cGMP signaling pathway, which has various functions, including neuronal plasticity, learning, and memory (Schmidt et al, 2002;Kaun et al, 2007;Wang et al, 2008;Reaume and Sokolowski, 2009;Francis et al, 2010). Our previous studies have revealed that for is required for visual pattern memory in the central complex of Drosophila (Wang et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

“…It is known that different Lola isoforms have distinct functions (Goeke et al, 2003;Spletter et al, 2007;Fukui et al, 2012;Southall et al, 2014). Therefore, three relatively well-studied Lola proteins (LolaA, LolaL, and LolaT) were tested for the physical association with PKG by coimmunoprecipitation experiments using Drosophila S2 cells.…”

Section: Pkg Physically Interacts With Lolat Both In Vitro and In Vivomentioning

confidence: 99%

“…As a key component of the cGMP signaling pathway, PKG is well known for its functions in cardiac protection, smooth muscle relaxation, neuronal plasticity, and learning and memory (Kaun et al, 2007;Wang et al, 2008;Francis et al, 2010;Kohn et al, 2013). However, little is known about the role of PKG in axon guidance.…”

Section: Introductionmentioning

confidence: 99%

“…In the CNS, Lola is required for repelling longitudinal axons away from the midline through augmenting the expression of the midline repellant Slit and axonal receptor Robo (Crowner et al, 2002). In the PNS, Lola promotes ISNb axon growth, in part by suppressing the expression of an actin nucleation factor, spire, and controls synapse formation through regulating the expression of glutamate receptors (Gates et al, 2011;Fukui et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

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cGMP-Dependent Protein Kinase Encoded byforagingRegulates Motor Axon Guidance inDrosophilaby Suppressing Lola Function

Peng

Wang

et al. 2016

J. Neurosci.

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Correct pathfinding and target recognition of a developing axon are exquisitely regulated processes that require multiple guidance factors. Among these factors, the second messengers, cAMP and cGMP, are known to be involved in establishing the guidance cues for axon growth through different intracellular signaling pathways. However, whether and how cGMP-dependent protein kinase (PKG) regulates axon guidance remains poorly understood. Here, we show that the motor axons of intersegmental nerve b (ISNb) in the Drosophila embryo display targeting defects during axon development in the absence of foraging ( for), a gene encoding PKG. In vivo tag expression revealed PKG to be present in the ventral nerve code at late embryonic stages, supporting its function in embryonic axon guidance. Mechanistic studies showed that the transcription factor longitudinal lacking (lola) genetically interacts with for. PKG physically associates with the LolaT isoform via the C-terminal zinc-finger-containing domain. Overexpression of PKG leads to the cytoplasmic retention of LolaT in S2 cells, suggesting a role for PKG in mediating the nucleocytoplasmic trafficking of Lola. Together, these findings reveal a novel function of PKG in regulating the establishment of neuronal connectivity by sequestering Lola in the cytoplasm.

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Section: Pkg Physically Interacts With Lolat Both In Vitro and In Vivosupporting

confidence: 58%

Section: Discussionmentioning

confidence: 99%

Section: Pkg Physically Interacts With Lolat Both In Vitro and In Vivomentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

cGMP-Dependent Protein Kinase Encoded byforagingRegulates Motor Axon Guidance inDrosophilaby Suppressing Lola Function

Peng

Wang

et al. 2016

J. Neurosci.

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Evidence for a hierarchical transcriptional circuit in Drosophila male germline involving testis‐specific TAF and two gene‐specific transcription factors, Mod and Acj6

et al. 2017

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Edited by Lukas Alfons HuberTo analyze transcription factors involved in gene regulation by testis-specific TAF (tTAF), tTAF-dependent promoters were mapped and analyzed in silico. Core promoters show decreased AT content, paucity of classical promoter motifs, and enrichment with translation control element CAAAATTY. Scanning of putative regulatory regions for known position frequency matrices identified 19 transcription regulators possibly contributing to tTAF-driven gene expression. Decreased male fertility associated with mutation in one of the regulators, Acj6, indicates its involvement in male reproduction. Transcriptome study of testes from male mutants for tTAF, Acj6, and previously characterized tTAF-interacting factor Modulo implies the existence of a regulatory hierarchy of tTAF, Modulo and Acj6, in which Modulo and/or Acj6 regulate one-third of tTAF-dependent genes.Keywords: Drosophila; gene-specific transcription regulator; hierarchical transcriptional circuit; spermatogenesis; testis-specific TAF During Drosophila spermatogenesis, spermatogonial cells born from male germline stem cells multiply through four rounds of mitotic divisions and differentiate into spermatocytes. Upon lengthy maturation, spermatocytes in turn proceed through meiotic divisions to generate round haploid spermatids. Completion of the meiosis itself and dramatic morphological transformation of spermatids into mature sperms require numerous structural and regulatory proteins, expression of which is mostly supported by highly active transcription in spermatocytes [1]. The testisspecific gene expression is usually activated in spermatocytes [2]. Furthermore, a wealth of male-sterile mutants identified so far block at the initiation of spermatid differentiation program in spermatocytes [3]. Thus, the regulatory network in the spermatocyte period warrants detailed analysis both as a striking example of vast cell type-specific transcription and as a molecular mechanism that underlies male fertility.To date, very few transcription factors are known to be essential for spermatocyte-specific gene expression. The most well-characterized group includes genes of the meiotic arrest class, which encode either testis-specific TATA-binding protein-associated factors (tTAFs) or components of testis meiotic arrest complex (tMAC), except that Achintya and Vismay constitute a distinct complex [2]. The tMAC complex controls expression of key G2-M cell cycle genes [4], and its Abbreviations cTFIID, canonical TFIID; PFMs, position frequency matrices; TAF, TATA-binding protein associated factors; tBRD, testis-specific bromodomain protein; TCE, translational control element; tMAC, testis meiotic arrest complex; TSSs, transcription start sites; tTAF, testis-specific TAF. 46FEBS Letters 592 (2018) 46-59 ª 2017 Federation of European Biochemical Societies disruption shows dramatic drop in transcription of over 1500 genes in testes, whose effect is broader than the tTAF disruption [2]. The five tTAFs identified thus far in the primary spermatocytes are als...

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Hindsight regulates photoreceptor axon targeting through transcriptional control of jitterbug/Filamin and multiple genes involved in axon guidance in Drosophila

Oliva

Molina-Fernandez

Maureira

et al. 2015

Developmental Neurobiology

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During axon targeting, a stereotyped pattern of connectivity is achieved by the integration of intrinsic genetic programs and the response to extrinsic long and short-range directional cues. How this coordination occurs is the subject of intense study. Transcription factors play a central role due to their ability to regulate the expression of multiple genes required to sense and respond to these cues during development. Here we show that the transcription factor HNT regulates layer-specific photoreceptor axon targeting in Drosophila through transcriptional control of jbug/Filamin and multiple genes involved in axon guidance and cytoskeleton organization.Using a microarray analysis we identified 235 genes whose expression levels were changed by HNT overexpression in the eye primordia. We analyzed nine candidate genes involved in cytoskeleton regulation and axon guidance, six of which displayed significantly altered gene expression levels in hnt mutant retinas. Functional analysis confirmed the role of OTK/PTK7 in photoreceptor axon targeting and uncovered Tiggrin, an integrin ligand, and Jbug/Filamin, a conserved actin- binding protein, as new factors that participate of photoreceptor axon targeting. Moreover, we provided in silico and molecular evidence that supports jbug/Filamin as a direct transcriptional target of HNT and that HNT acts partially through Jbug/Filamin in vivo to regulate axon guidance. Our work broadens the understanding of how HNT regulates the coordinated expression of a group of genes to achieve the correct connectivity pattern in the Drosophila visual system. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 75: 1018-1032, 2015.

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The transcriptional regulator lola is required for stem cell maintenance and germ cell differentiation in the Drosophila testis

Cited by 26 publications

References 40 publications

cGMP-Dependent Protein Kinase Encoded byforagingRegulates Motor Axon Guidance inDrosophilaby Suppressing Lola Function

cGMP-Dependent Protein Kinase Encoded byforagingRegulates Motor Axon Guidance inDrosophilaby Suppressing Lola Function

Evidence for a hierarchical transcriptional circuit in Drosophila male germline involving testis‐specific TAF and two gene‐specific transcription factors, Mod and Acj6

Hindsight regulates photoreceptor axon targeting through transcriptional control of jitterbug/Filamin and multiple genes involved in axon guidance in Drosophila

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