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  • 1.
    Hosono, Chie
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Matsuda, Ryo
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Adryan, Boris
    Samakovlis, Christos
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. University of Giessen, Germany.
    Transient junction anisotropies adjust 3-dimensional cell polarization to tissue geometryManuscript (preprint) (Other academic)
  • 2.
    Hosono, Chie
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Matsuda, Ryo
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Adryan, Boris
    Samakovlis, Christos
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. ECCPS, University of Giessen, Germany.
    Transient junction anisotropies orient annular cell polarization in the Drosophila airway tubes2015In: Nature Cell Biology, ISSN 1465-7392, E-ISSN 1476-4679, Vol. 17, no 12, p. 1569-1576Article in journal (Refereed)
    Abstract [en]

    In contrast to planes, three-dimensional (3D) structures such as tubes are physically anisotropic. Tubular organs exhibit a striking orientation of landmarks according to the physical anisotropy of the 3D shape(1-4), in addition to planar cell polarization(5,6). However, the influence of 3D tissue topography on the constituting cells remains underexplored(7-9). Here, we identify a regulatory network polarizing cellular biochemistry according to the physical anisotropy of the 3D tube geometry (tube cell polarization) by a genome-wide, tissue-specific RNAi screen. During Drosophila airway remodelling, each apical cellular junction is equipotent to establish perpendicular actomyosin cables, irrespective of the longitudinal or transverse tube axis. A dynamic transverse enrichment of atypical protein kinase C (aPKC) shifts the balance and transiently targets activated small GTPase RhoA, myosin phosphorylation and Rab11 vesicle trafficking to longitudinal junctions. We propose that the PAR complex translates tube physical anisotropy into longitudinal junctional anisotropy, where cell cell communication aligns the contractile cytoskeleton of neighbouring cells.

  • 3.
    Matsuda, Ryo
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Revisiting cell specification and differentiation in the Drosophila airways, an insect organ homologous to our lung and blood vessels2015Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Oxygen is essential for life. Aquatic ancestral animal species are thought to have independently terrestrialized and invented distinct strategies for efficient oxygen supply. The respiratory system of vertebrates like us is composed of lungs connected to the vasculature while insects have a single system delivering air directly to internal tissues. In spite of their different evolutionary histories, the formation of these different tubular networks is thought to share many cellular, genetic and molecular principles. Here, in register with preceding studies, I briefly introduce the projects of my co-authors and me, addressing several new aspects of specification and differentiation of the Drosophila airways.

    The airway primordia are specified at the lateral ectoderm of each side of the embryo as 10 groups of epithelial cells. These cells coordinately invaginate from the 2-dimensional (2D) ectodermal sheet to form 3D primitive tubes. The most proximal cells to the epidermis take the pluripotent cell fate and later generate most of the pupal and adult airways. Distal cells ramify to establish the primary branches and some neighboring branches fuse, interconnecting the network. Establishing these basic architectures, the tubular network matures into functional airways, attaining proper tube sizes in diameter and length, producing an annular-ridged lining of exoskeleton to avoid tube collapse and finally filling the system with gas.

    First, I present airway-promoting functions of factors that were previously assigned to repress the airway fate. Then, I present genetic frameworks discriminating between 3 ground cell fates and the more derived cell fates: A) the proximal pluripotent cells vs. the distal more differentiated cells, B) the visceral branch vs. the signal-induced primary branches and C) the 1st metamere vs. the more posterior metameres. Lastly, I present our efforts to identify genes converting the airway tubes into a functional respiratory system.

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  • 4.
    Matsuda, Ryo
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hosono, Chie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Saigo, Kaoru
    Samakovlis, Christos
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. University of Giessen, Germany.
    Antagonistic interactions between the Emx ortholog Empty spiracle with Wingless/WNT, Dpp/BMP and Hox proteins induce branch-specific apoptotic pruning in the Drosophila airwaysManuscript (preprint) (Other academic)
  • 5.
    Matsuda, Ryo
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hosono, Chie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Saigo, Kaoru
    Samakovlis, Christos
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. University of Giessen, Germany.
    The Intersection of the Extrinsic Hedgehog and WNT/Wingless Signals with the Intrinsic Hox Code Underpins Branching Pattern and Tube Shape Diversity in the Drosophila Airways2015In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 11, no 1, article id e1004929Article in journal (Refereed)
    Abstract [en]

    The tubular networks of the Drosophila respiratory system and our vasculature show distinct branching patterns and tube shapes in different body regions. These local variations are crucial for organ function and organismal fitness. Organotypic patterns and tube geometries in branched networks are typically controlled by variations of extrinsic signaling but the impact of intrinsic factors on branch patterns and shapes is not well explored. Here, we show that the intersection of extrinsic hedgehog(hh) and WNT/wingless (wg) signaling with the tube-intrinsic Hox code of distinct segments specifies the tube pattern and shape of the Drosophila airways. In the cephalic part of the airways, hh signaling induces expression of the transcription factor (TF) knirps (kni) in the anterior dorsal trunk (DTa1). kni represses the expression of another TF spalt major (salm), making DTa1 a narrow and long tube. In DTa branches of more posterior metameres, Bithorax Complex (BX-C) Hox genes autonomously divert hh signaling from inducing kni, thereby allowing DTa branches to develop as salm-dependent thick and short tubes. Moreover, the differential expression of BX-C genes is partly responsible for the anterior-to-posterior gradual increase of the DT tube diameter through regulating the expression level of Salm, a transcriptional target of WNT/wg signaling. Thus, our results highlight how tube intrinsic differential competence can diversify tube morphology without changing availabilities of extrinsic factors.

  • 6.
    Matsuda, Ryo
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hosono, Chie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Samakovlis, Christos
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. University of Giessen, Germany.
    Saigo, Kaoru
    A genetic basis for pluripotent versus differentiated cell fate selection during early development of the Drosophila airwaysManuscript (preprint) (Other academic)
  • 7.
    Matsuda, Ryo
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hosono, Chie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Samakovlis, Christos
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. University of Giessen, Germany.
    Saigo, Kaoru
    Decapentaplegic/BMP and dEGFR promote the airway cell fate in DrosophilaManuscript (preprint) (Other academic)
  • 8.
    Matsuda, Ryo
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hosono, Chie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Samakovlis, Christos
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Stockholm University, Science for Life Laboratory (SciLifeLab). Justus Liebig University of Giessen, Germany.
    Saigo, Kaoru
    Multipotent versus differentiated cell fate selection in the developing Drosophila airways2015In: eLIFE, E-ISSN 2050-084X, Vol. 4, article id e09646Article in journal (Refereed)
    Abstract [en]

    Developmental potentials of cells are tightly controlled at multiple levels. The embryonic Drosophila airway tree is roughly subdivided into two types of cells with distinct developmental potentials: a proximally located group of multipotent adult precursor cells (P-fate) and a distally located population of more differentiated cells (D-fate). We show that the GATA-family transcription factor (TF) Grain promotes the P-fate and the POU-homeobox TF Ventral veinless (Vvl/Drifter/U-turned) stimulates the D-fate. Hedgehog and receptor tyrosine kinase (RTK) signaling cooperate with Vvl to drive the D-fate at the expense of the P-fate while negative regulators of either of these signaling pathways ensure P-fate specification. Local concentrations of Decapentaplegic/BMP, Wingless/Wnt, and Hedgehog signals differentially regulate the expression of D-factors and P-factors to transform an equipotent primordial field into a concentric pattern of radially different morphogenetic potentials, which gradually gives rise to the distal-proximal organization of distinct cell types in the mature airway.

  • 9.
    Tsarouhas, Vasilios
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Liu, Dan
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Tsikala, Georgia
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Fedoseienko, Alina
    Zinn, Kai
    Matsuda, Ryo
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Billadeau, Daniel D.
    Samakovlis, Christos
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Stockholm University, Science for Life Laboratory (SciLifeLab). Justus Liebig University of Giessen, Germany.
    WASH phosphorylation balances endosomal versus cortical actin network integrities during epithelial morphogenesis2019In: Nature Communications, E-ISSN 2041-1723, Vol. 10, article id 2193Article in journal (Refereed)
    Abstract [en]

    Filamentous actin (F-actin) networks facilitate key processes like cell shape control, division, polarization and motility. The dynamic coordination of F-actin networks and its impact on cellular activities are poorly understood. We report an antagonistic relationship between endosomal F-actin assembly and cortical actin bundle integrity during Drosophila airway maturation. Double mutants lacking receptor tyrosine phosphatases (PTP) Ptp10D and Ptp4E, clear luminal proteins and disassemble apical actin bundles prematurely. These defects are counterbalanced by reduction of endosomal trafficking and by mutations affecting the tyrosine kinase Btk29A, and the actin nucleation factor WASH. Btk29A forms protein complexes with Ptp10D and WASH, and Btk29A phosphorylates WASH. This phosphorylation activates endosomal WASH function in flies and mice. In contrast, a phospho-mimetic WASH variant induces endosomal actin accumulation, premature luminal endocytosis and cortical F-actin disassembly. We conclude that PTPs and Btk29A regulate WASH activity to balance the endosomal and cortical F-actin networks during epithelial tube maturation.

  • 10.
    Yao, Liqun
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Wang, Shenqiu
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Sloan Kettering Institute, USA.
    Dai, Qi
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Sloan Kettering Institute, USA.
    Orzechowski-Westholm, Jakub
    Matsuda, Ryo
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hosono, Chie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Bray, Sarah
    Lai, Eric C.
    Samakovlis, Christos
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Stockholm University, Science for Life Laboratory (SciLifeLab). Universities of Giessen and Marburg Lung Center (UGMLC), Germany.
    Genome-wide identification of Grainy head target genes in Drosophila reveals complex regulatory interactions between Grh and the POU-domain transcription factor, VvlManuscript (preprint) (Other academic)
  • 11.
    Yao, Liqun
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Wang, Shenqiu
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Sloan-Kettering Institute, USA.
    Westholm, Jakub O.
    Dai, Qi
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Sloan-Kettering Institute, USA.
    Matsuda, Ryo
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hosono, Chie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Bray, Sarah
    Lai, Eric C.
    Samakovlis, Christos
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute. Stockholm University, Science for Life Laboratory (SciLifeLab). UGMLC, Germany.
    Genome-wide identification of Grainy head targets in Drosophila reveals regulatory interactions with the POU domain transcription factor Vvl2017In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 144, no 17, p. 3145-3155Article in journal (Refereed)
    Abstract [en]

    Grainy head (Grh) is a conserved transcription factor (TF) controlling epithelial differentiation and regeneration. To elucidate Grh functions we identified embryonic Grh targets by ChIP-seq and gene expression analysis. We show that Grh controls hundreds of target genes. Repression or activation correlates with the distance of Grh-binding sites to the transcription start sites of its targets. Analysis of 54 Grh-responsive enhancers during development and upon wounding suggests cooperation with distinct TFs in different contexts. In the airways, Grh-repressed genes encode key TFs involved in branching and cell differentiation. Reduction of the POU domain TF Ventral veins lacking (Vvl) largely ameliorates the airway morphogenesis defects of grh mutants. Vvl and Grh proteins additionally interact with each other and regulate a set of common enhancers during epithelial morphogenesis. We conclude that Grh and Vvl participate in a regulatory network controlling epithelial maturation.

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