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Filopodia-based contact stimulated collective migration drives tissue morphogenesis [article]

Maik Bischoff, Renate Renkawitz-Pohl, Sven Bogdan
2020 bioRxiv   pre-print
Cells migrate collectively to form tissues and organs during morphogenesis. Contact inhibition of locomotion (CIL) drives collective migration by inhibiting lamellipodial protrusions at cell-cell contacts and promoting polarization at the leading edge. Here, we report on a CIL-related collective cell behavior of myotubes that lack lamellipodial protrusions, but instead use filopodia to move as a cohesive cluster in a formin-dependent manner. Genetic, pharmacological and mechanical perturbation
more » ... nalyses reveal essential roles of Rac2, Cdc42 and Rho1 in myotube migration. They differentially control not only protrusion dynamics but also cell-matrix adhesion formation. Here, active Rho1 GTPase localizes at retracting free edge filopodia. Rok-dependent actomyosin contractility does not mediate a contraction of protrusions at cell-cell contacts but likely plays an important role in the constriction of supracellular actin cables. We propose that contact-dependent asymmetry of cell-matrix adhesion drives directional movement, whereas contractile actin cables contribute to the integrity of the migrating cell cluster.
doi:10.1101/2020.10.19.345082 fatcat:6alor5762nfddic4nygpol63p4

Characterization of cloned ribosomal DNA from Drosophila hydei

Renate Renkawitz-Pohl, Karl Heinz Glätzer, Werner Kunz
1980 Nucleic Acids Research  
MATERIAL AND METHODS Preparation and Purification of D. hydei DNA Nuclei from frozen adult flies of different genotypes were isolated as described by Renkawitz (8) and lyzed for 15 min at 65°C in Marmur  ... 
doi:10.1093/nar/8.20.4593 pmid:6255425 pmcid:PMC324373 fatcat:jfzc2zlhhbfurisis4uh2okdnq

Chromatin dynamics during spermiogenesis

Christina Rathke, Willy M. Baarends, Stephan Awe, Renate Renkawitz-Pohl
2014 Biochimica et Biophysica Acta. Gene Regulatory Mechanisms  
We thank Rainer Renkawitz for the critical reading of the manuscript and Katja Gessner for the excellent secretarial assistance and graphic design.  ... 
doi:10.1016/j.bbagrm.2013.08.004 pmid:24091090 fatcat:hgafonx23bg5fgn6ktceominry

Filopodia-based contact stimulation of cell migration drives tissue morphogenesis

Maik C. Bischoff, Sebastian Lieb, Renate Renkawitz-Pohl, Sven Bogdan
2021 Nature Communications  
AbstractCells migrate collectively to form tissues and organs during morphogenesis. Contact inhibition of locomotion (CIL) drives collective migration by inhibiting lamellipodial protrusions at cell–cell contacts and promoting polarization at the leading edge. Here, we report a CIL-related collective cell behavior of myotubes that lack lamellipodial protrusions, but instead use filopodia to move as a cohesive cluster in a formin-dependent manner. We perform genetic, pharmacological and
more » ... l perturbation analyses to reveal the essential roles of Rac2, Cdc42 and Rho1 in myotube migration. These factors differentially control protrusion dynamics and cell–matrix adhesion formation. We also show that active Rho1 GTPase localizes at retracting free edge filopodia and that Rok-dependent actomyosin contractility does not mediate a contraction of protrusions at cell–cell contacts, but likely plays an important role in the constriction of supracellular actin cables. Based on these findings, we propose that contact-dependent asymmetry of cell–matrix adhesion drives directional movement, whereas contractile actin cables contribute to the integrity of the migrating cell cluster.
doi:10.1038/s41467-020-20362-2 pmid:33542237 fatcat:7rl5qjczszcenbm756asowr6ay

The Drosophila insulator proteins CTCF and CP190 link enhancer blocking to body patterning

Man Mohan, Marek Bartkuhn, Martin Herold, Angela Philippen, Nina Heinl, Imke Bardenhagen, Joerg Leers, Robert A H White, Renate Renkawitz-Pohl, Harald Saumweber, Rainer Renkawitz
2007 EMBO Journal  
Insulator sequences guide the function of distantly located enhancer elements to the appropriate target genes by blocking inappropriate interactions. In Drosophila, five different insulator binding proteins have been identified, Zw5, BEAF-32, GAGA factor, Su(Hw) and dCTCF. Only dCTCF has a known conserved counterpart in vertebrates. Here we find that the structurally related factors dCTCF and Su(Hw) have distinct binding targets. In contrast, the Su(Hw) interacting factor CP190 largely
more » ... d with dCTCF binding sites and interacts with dCTCF. Binding of dCTCF to targets requires CP190 in many cases, whereas others are independent of CP190. Analysis of the bithorax complex revealed that six of the borders between the parasegment specific regulatory domains are bound by dCTCF and by CP190 in vivo. dCTCF null mutations affect expression of Abdominal-B, cause pharate lethality and a homeotic phenotype. A short pulse of dCTCF expression during larval development rescues the dCTCF loss of function phenotype. Overall, we demonstrate the importance of dCTCF in fly development and in the regulation of abdominal segmentation.
doi:10.1038/sj.emboj.7601851 pmid:17805343 pmcid:PMC2230845 fatcat:lzkblwqjyranrnom4ehs4qsxz4

Prtl99C Acts Together with Protamines and Safeguards Male Fertility in Drosophila

Zeynep Eren-Ghiani, Christina Rathke, Ina Theofel, Renate Renkawitz-Pohl
2015 Cell Reports  
Renkawitz-Pohl Correspondence renkawit@biologie.uni-marburg.de In Brief Eren-Ghiani et al. find that Prtl99C acts together with protamines in Drosophila chromatin condensation in sperm and is pivotal  ...  Drosophila d Protamines cannot be replaced by Mst77F or Prtl99C d Prtl99C and protamines act additively to form highly compact paternal chromatin Authors Zeynep Eren-Ghiani, Christina Rathke, Ina Theofel, Renate  ...  The replacement of histones with protamines is gradual, as shown by live-cell imaging of Drosophila male germ cells (Awe and Renkawitz-Pohl, 2010) .  ... 
doi:10.1016/j.celrep.2015.11.023 pmid:26673329 fatcat:uuu5ggewnbgtxdn7yomkcpi6qe

A new level of plasticity:Drosophilasmooth-like testes muscles compensate failure of myoblast fusion

Jessica Kuckwa, Katharina Fritzen, Detlev Buttgereit, Silke Rothenbusch-Fender, Renate Renkawitz-Pohl
2015 Development  
., 2010; Önel and Renkawitz-Pohl, 2009 ). Furthermore, defective morphogenesis of the reproductive system can induce male sterility (Linnemannstons et al., 2014) .  ... 
doi:10.1242/dev.126730 pmid:26657767 pmcid:PMC4725342 fatcat:m463v3dnlvazdmp6mhal2lckxm

Two distinct intervening sequences in different ribosomal DNA repeat units of Sciara coprophila

Renate Renkawitz-Pohl, Lloyd Matsumoto, Susan A. Gerbi
1981 Nucleic Acids Research  
Gourse, and Rainer Renkawitz for helpful comments and discussion. We thank Mrs. Carol King for typing this manu-  ... 
doi:10.1093/nar/9.15.3747 pmid:7279671 pmcid:PMC327389 fatcat:jncchelscvaqlf6dvluhcdviyy

The HMG-box-containing proteins tHMG-1 and tHMG-2 interact during the histone-to-protamine transition in Drosophila spermatogenesis

Stefanie M.K. Gärtner, Silke Rothenbusch, Melanie K. Buxa, Ina Theofel, Rainer Renkawitz, Christina Rathke, Renate Renkawitz-Pohl
2015 European Journal of Cell Biology  
In vivo imaging using Drosophila cyst cultures Cyst cultures of double-transgenic flies carrying tHMG-1-eGFP and H2AvD-RFP were established as described in Awe and Renkawitz-Pohl (2010) and Gärtner  ...  containing 16 sister cells that progress together through spermatogenesis until individualization -from a fly strain expressing tHMG-1-eGFP and H2AvD-RFP were isolated and taken into culture (Awe and Renkawitz-Pohl  ... 
doi:10.1016/j.ejcb.2014.10.005 pmid:25464903 fatcat:bc2mrf23ozbi7o67kkp4num4c4

CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator

Hanlim Moon, Galina Filippova, Dmitry Loukinov, Elena Pugacheva, Qi Chen, Sheryl T Smith, Adam Munhall, Britta Grewe, Marek Bartkuhn, Rüdiger Arnold, Les J Burke, Renate Renkawitz-Pohl (+4 others)
2005 EMBO Reports  
Eukaryotic transcriptional regulation often involves regulatory elements separated from the cognate genes by long distances, whereas appropriately positioned insulator or enhancer-blocking elements shield promoters from illegitimate enhancer action. Four proteins have been identified in Drosophila mediating enhancer blocking-Su(Hw), Zw5, BEAF32 and GAGA factor. In vertebrates, the single protein CTCF, with 11 highly conserved zinc fingers, confers enhancer blocking in all known chromatin
more » ... ors. Here, we characterize an orthologous CTCF factor in Drosophila with a similar domain structure, binding site specificity and transcriptional repression activity as in vertebrates. In addition, we demonstrate that one of the insulators (Fab-8) in the Drosophila Abdominal-B locus mediates enhancer blocking by dCTCF. Therefore, the enhancer-blocking protein CTCF and, most probably, the mechanism of enhancer blocking mediated by this remarkably versatile factor are conserved from Drosophila to humans.
doi:10.1038/sj.embor.7400334 pmid:15678159 pmcid:PMC1299244 fatcat:iw6af42ezbdjpct7btxtvvwjzy

Tinman Regulates the Transcription of the β3 tubulin Gene (βTub60D) in the Dorsal Vessel of Drosophila

Thomas Kremser, Kathleen Gajewski, Robert A. Schulz, Renate Renkawitz-Pohl
1999 Developmental Biology  
During Drosophila embryogenesis, the ␤3 tubulin gene is expressed in the visceral and somatic mesoderm as well as in the dorsal vessel. Transcription of the gene is limited to four pairs of cardioblasts per segment. Here we show that its expression in the dorsal vessel (dv) is mediated by a 333-bp enhancer located upstream of the gene. The homeodomain protein Tinman is also expressed in these cardioblasts, implying that Tinman might be a key regulator of the ␤3 tubulin gene. Gel retardation and
more » ... footprint assays indeed revealed two Tinman binding sites within the dv-specific enhancer. We analyzed the relevance of the Tinman binding sites in a transgenic fly assay and observed distinct functions for both sites. The BS Tin-1460 site is absolutely required for expression in cardioblasts, while BS Tin-1425 is needed for high-level expression. Thus, these two Tinman binding sites act in concert to drive ␤3 tubulin gene expression during heart development. Tinman initially functions in the specification of visceral mesoderm and heart progenitors, but remains expressed in cardioblasts until dorsal closure. Overall, our data demonstrate a late function for Tinman in the regulation of ␤3 tubulin gene expression in the forming heart of Drosophila. FIG. 5. In vitro binding of the GST-Tinman fusion protein to BS Tin-1460 of the ␤3 tubulin dorsal vessel enhancer. (A) The Ϫ1460 sequence is a specific binding site for the Tinman protein. Gel retardation assay was done in the presence of GST-Tinman protein and 32 P-end-labeled double-stranded oligonucleotide Ϫ1460 ϩ/Ϫ. The specificity of the formed complex (arrow) is demonstrated by competition using 50-, 100-, and 150-fold molar excess of unlabeled Ϫ1460 ϩ/Ϫ (lanes 3, 4, and 5) in comparison to nonspecific competition using B1RE1CϩD as a double-stranded competitor oligonucleotide (lanes 6, 7, and 8). (B) The specificity of this DNA-protein complex was further demonstrated by adding different amounts of anti-GST antibody to the gel mobility shift reactions. The probe Ϫ1460 ϩ/Ϫ was incubated with the GST-Tinman protein and 150 (lane 3), 75 (lane 4), 36 (lane 5), or 18 ng/l (lane 6) anti-GST antibody during the binding reactions. The protein-DNA complex is indicated by an arrow, the antibody-induced supershifted band, located mostly in the origins of the gel, is marked by a double arrow.
doi:10.1006/dbio.1999.9425 pmid:10588882 fatcat:ge2re54qtjecrfp33xj7io3czm

Tethering Membrane Fusion: Common and Different Players in Myoblasts and at the Synapse

Susanne Filiz Önel, Marco B. Rust, Ralf Jacob, Renate Renkawitz-Pohl
2014 Journal of neurogenetics  
The rings expand during the fusion process, which suggests that fusion takes place within the area restricted by these IgSFs ( Ö nel & Renkawitz-Pohl, 2009; Ö nel et al., 2011) .  ...  Recent progress in understanding the intercellular fusion of myoblasts, which is essential for building muscles, has been achieved by using the powerful genetic analyses of Drosophila ( Ö nel and Renkawitz-Pohl  ... 
doi:10.3109/01677063.2014.936014 pmid:24957080 pmcid:PMC4245166 fatcat:uv3mv5c75jg7tjdf43dg7ftn74

Multimerization of Drosophila sperm protein Mst77F causes a unique condensed chromatin structure

Nils Kost, Sophie Kaiser, Yogesh Ostwal, Dietmar Riedel, Alexandra Stützer, Miroslav Nikolov, Christina Rathke, Renate Renkawitz-Pohl, Wolfgang Fischle
2015 Nucleic Acids Research  
Despite insights on the cellular level, the molecular details of chromatin reorganization in sperm development, which involves replacement of histone proteins by specialized factors to allow ultra most condensation of the genome, are not well understood. Protamines are dispensable for DNA condensation during Drosophila post-meiotic spermatogenesis. Therefore, we analyzed the interaction of Mst77F, another very basic testis-specific protein with chromatin and DNA as well as studied the molecular
more » ... consequences of such binding. We show that Mst77F on its own causes severe chromatin and DNA aggregation. An intrinsically unstructured domain in the C-terminus of Mst77F binds DNA via electrostatic interaction. This binding results in structural reorganization of the domain, which induces interaction with an N-terminal region of the protein. Via putative cooperative effects Mst77F is induced to multimerize in this state causing DNA aggregation. In agreement, overexpression of Mst77F results in chromatin aggregation in fly sperm. Based on these findings we postulate that Mst77F is crucial for sperm development by giving rise to a unique condensed chromatin structure.
doi:10.1093/nar/gkv015 pmid:25735749 pmcid:PMC4381051 fatcat:tarhi2wdpbbavdt5hrcw7k6gmm

Nejire/dCBP-mediated histone H3 acetylation during spermatogenesis is essential for male fertility in Drosophila melanogaster

Tim Hundertmark, Stefanie M. K. Gärtner, Christina Rathke, Renate Renkawitz-Pohl, Mary Bryk
2018 PLoS ONE  
Author Contributions Conceptualization: Renate Renkawitz-Pohl.  ...  Acknowledgments We thank Igor Macinkovic for advice for qPCR experiments, Rainer Renkawitz for critical reading of the manuscript.  ... 
doi:10.1371/journal.pone.0203622 pmid:30192860 pmcid:PMC6128621 fatcat:xq4t2gy5zffppm5huqz2mluad4

Three levels of regulation lead to protamine and Mst77F expression in Drosophila

Bridlin Barckmann, Xin Chen, Sophie Kaiser, Sunil Jayaramaiah-Raja, Christina Rathke, Christine Dottermusch-Heidel, Margaret T. Fuller, Renate Renkawitz-Pohl
2013 Developmental Biology  
Thus, protB mRNAs are stored in an untranslated state up to 6 days (Awe and Renkawitz-Pohl, 2010) .  ...  This is a typical feature for translational control of certain transcripts during spermatogenesis in Drosophila (for a review, see Renkawitz-Pohl et al., 2005) .  ... 
doi:10.1016/j.ydbio.2013.02.018 pmid:23466740 pmcid:PMC4154633 fatcat:zb5u2jp35jfn3hfo4tzxkka344
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