#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#
preLekára.sk / Odborné časopisy / PLOS Genetics / 2014 - 1

Notch Controls Cell Adhesion in the Drosophila Eye

English version České info

Sporadic evidence suggests Notch is involved in cell adhesion. However, the underlying mechanism is unknown. Here I have investigated an epithelial remodeling process in the Drosophila eye in which two primary pigment cells (PPCs) with a characteristic ‘kidney’ shape enwrap and eventually isolate a group of cone cells from inter-ommatidial cells (IOCs). This paper shows that in the developing Drosophila eye the ligand Delta was transcribed in cone cells and Notch was activated in the adjacent PPC precursors. In the absence of Notch, emerging PPCs failed to enwrap cone cells, and hibris (hbs) and sns, two genes coding for adhesion molecules of the Nephrin group that mediate preferential adhesion, were not transcribed in PPC precursors. Conversely, activation of Notch in single IOCs led to ectopic expression of hbs and sns. By contrast, in a single IOC that normally transcribes rst, a gene coding for an adhesion molecule of the Neph1 group that binds Hbs and Sns, activation of Notch led to a loss of rst transcription. In addition, in a Notch mutant where two emerging PPCs failed to enwrap cone cells, expression of hbs in PPC precursors restored the ability of these cells to surround cone cells. Further, expression of hbs or rst in a single rst -⁠ or hbs-expressing cell, respectively, led to removal of the counterpart from the membrane within the same cell through cis-interaction and forced expression of Rst in all hbs-expressing PPCs strongly disrupted the remodeling process. Finally, a loss of both hbs and sns in single PPC precursors led to constriction of the apical surface that compromised the ‘kidney’ shape of PPCs. Taken together, these results indicate that cone cells utilize Notch signaling to instruct neighboring PPC precursors to surround them and Notch controls the remodeling process by differentially regulating four adhesion genes.

Vyšlo v časopise: Notch Controls Cell Adhesion in the Drosophila Eye. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004087
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004087

Souhrn

Sporadic evidence suggests Notch is involved in cell adhesion. However, the underlying mechanism is unknown. Here I have investigated an epithelial remodeling process in the Drosophila eye in which two primary pigment cells (PPCs) with a characteristic ‘kidney’ shape enwrap and eventually isolate a group of cone cells from inter-ommatidial cells (IOCs). This paper shows that in the developing Drosophila eye the ligand Delta was transcribed in cone cells and Notch was activated in the adjacent PPC precursors. In the absence of Notch, emerging PPCs failed to enwrap cone cells, and hibris (hbs) and sns, two genes coding for adhesion molecules of the Nephrin group that mediate preferential adhesion, were not transcribed in PPC precursors. Conversely, activation of Notch in single IOCs led to ectopic expression of hbs and sns. By contrast, in a single IOC that normally transcribes rst, a gene coding for an adhesion molecule of the Neph1 group that binds Hbs and Sns, activation of Notch led to a loss of rst transcription. In addition, in a Notch mutant where two emerging PPCs failed to enwrap cone cells, expression of hbs in PPC precursors restored the ability of these cells to surround cone cells. Further, expression of hbs or rst in a single rst -⁠ or hbs-expressing cell, respectively, led to removal of the counterpart from the membrane within the same cell through cis-interaction and forced expression of Rst in all hbs-expressing PPCs strongly disrupted the remodeling process. Finally, a loss of both hbs and sns in single PPC precursors led to constriction of the apical surface that compromised the ‘kidney’ shape of PPCs. Taken together, these results indicate that cone cells utilize Notch signaling to instruct neighboring PPC precursors to surround them and Notch controls the remodeling process by differentially regulating four adhesion genes.

Zdroje

1. BaroloS, PosakonyJW (2002) Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev 16 : 1167–1181.

2. DahmannC, BaslerK (1999) Compartment boundaries: at the edge of development. Trends Genet 15 : 320–326.

3. IrvineKD, VogtTF (1997) Dorsal-ventral signaling in limb development. Curr Opin Cell Biol 9 : 867–876.

4. CaganRL, ReadyDF (1989) Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev 3 : 1099–1112.

5. HoppePE, GreenspanRJ (1986) Local function of the Notch gene for embryonic ectodermal pathway choice in Drosophila. Cell 46 : 773–783.

6. HoltfreterJ (1939) Gewebeaffinität, ein Mittel der embryonal Formbildung. Arch Exptl Zellforsch Gewebezucht 23 : 169–209.

7. HoltfreterJ (1944) A study of the mechanics of gastrulation: Part II. J Exp Zool 95 : 171–212.

8. SteinbergMS (1963) Reconstruction of tissues by dissociated cells. Some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation. Science 141 : 401–408.

9. SteinbergMS (1970) Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. J Exp Zool 173 : 395–433.

10. GodtD, TepassU (1998) Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395 : 387–391.

11. Gonzalez-ReyesA, St JohnstonD (1998) The Drosophila AP axis is polarised by the cadherin-mediated positioning of the oocyte. Development 125 : 3635–3644.

12. HayashiT, CarthewRW (2004) Surface mechanics mediate pattern formation in the developing retina. Nature 431 : 647–652.

13. PriceSR, De Marco GarciaNV, RanschtB, JessellTM (2002) Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109 : 205–216.

14. BaoS, CaganR (2005) Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye. Dev Cell 8 : 925–935.

15. FischbachKF, LinneweberGA, AndlauerTF, HertensteinA, BonengelB, et al. (2009) The irre cell recognition module (IRM) proteins. J Neurogenet 23 : 48–67.

16. Garcia-BellidoA, MerriamJR (1969) Cell lineage of the imaginal discs in Drosophila gynandromorphs. J Exp Zool 170 : 61–75.

17. ShellenbargerDL, MohlerJD (1975) Temperature-sensitive mutations of the notch locus in Drosophila melanogaster. Genetics 81 : 143–162.

18. LarsonDE, LibermanZ, CaganRL (2008) Cellular behavior in the developing Drosophila pupal retina. Mech Dev 125 : 223–232.

19. FehonRG, JohansenK, RebayI, Artavanis-TsakonasS (1991) Complex cellular and subcellular regulation of notch expression during embryonic and imaginal development of Drosophila: implications for notch function. J Cell Biol 113 : 657–669.

20. KoohPJ, FehonRG, MuskavitchMA (1993) Implications of dynamic patterns of Delta and Notch expression for cellular interactions during Drosophila development. Development 117 : 493–507.

21. ParksAL, TurnerFR, MuskavitchMA (1995) Relationships between complex Delta expression and the specification of retinal cell fates during Drosophila eye development. Mech Dev 50 : 201–216.

22. FurriolsM, BrayS (2001) A model Notch response element detects Suppressor of Hairless-dependent molecular switch. Curr Biol 11 : 60–64.

23. BaoS, FischbachKF, CorbinV, CaganRL (2010) Preferential adhesion maintains separation of ommatidia in the Drosophila eye. Dev Biol 344 : 948–956.

24. StruhlG, FitzgeraldK, GreenwaldI (1993) Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74 : 331–345.

25. FuW, NollM (1997) The Pax2 homolog sparkling is required for development of cone and pigment cells in the Drosophila eye. Genes Dev 11 : 2066–2078.

26. Artavanis-TsakonasS, RandMD, LakeRJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284 : 770–776.

27. JacobsenTL, BrennanK, AriasAM, MuskavitchMA (1998) Cis-interactions between Delta and Notch modulate neurogenic signalling in Drosophila. Development 125 : 4531–4540.

28. MillerAC, LyonsEL, HermanTG (2009) cis-Inhibition of Notch by endogenous Delta biases the outcome of lateral inhibition. Curr Biol 19 : 1378–1383.

29. NagarajR, BanerjeeU (2007) Combinatorial signaling in the specification of primary pigment cells in the Drosophila eye. Development 134 : 825–831.

30. SinghJ, MlodzikM (2012) Hibris, a Drosophila nephrin homolog, is required for presenilin-mediated Notch and APP-like cleavages. Dev Cell 23 : 82–96.

31. ApitzH, KambacheldM, HohneM, RamosRG, StraubeA, et al. (2004) Identification of regulatory modules mediating specific expression of the roughest gene in Drosophila melanogaster. Dev Genes Evol 214 : 453–459.

32. LeeT, LuoL (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22 : 451–461.

33. SchneiderT, ReiterC, EuleE, BaderB, LichteB, et al. (1995) Restricted expression of the irreC-rst protein is required for normal axonal projections of columnar visual neurons. Neuron 15 : 259–271.

34. BourBA, ChakravartiM, WestJM, AbmayrSM (2000) Drosophila SNS, a member of the immunoglobulin superfamily that is essential for myoblast fusion. Genes Dev 14 : 1498–1511.

35. SchneiderCA, RasbandWS, EliceiriKW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9 : 671–675.

Štítky
Genetika Reprodukčná medicína
Článek How Much Is That in Dog Years? The Advent of Canine Population Genomics
Článek The Sense and Sensibility of Strand Exchange in Recombination Homeostasis
Článek Unwrapping Bacteria
Článek DNA Methylation Changes Separate Allergic Patients from Healthy Controls and May Reflect Altered CD4 T-Cell Population Structure
Článek Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species
Článek Translation Enhancing ACA Motifs and Their Silencing by a Bacterial Small Regulatory RNA
Článek Relationship Estimation from Whole-Genome Sequence Data
Článek Genetic Models of Apoptosis-Induced Proliferation Decipher Activation of JNK and Identify a Requirement of EGFR Signaling for Tissue Regenerative Responses in
Článek ComEA Is Essential for the Transfer of External DNA into the Periplasm in Naturally Transformable Cells
Článek Loss and Recovery of Genetic Diversity in Adapting Populations of HIV
Článek Bioelectric Signaling Regulates Size in Zebrafish Fins
Článek Defining NELF-E RNA Binding in HIV-1 and Promoter-Proximal Pause Regions
Článek Loss of Histone H3 Methylation at Lysine 4 Triggers Apoptosis in
Článek Cell-Cycle Dependent Expression of a Translocation-Mediated Fusion Oncogene Mediates Checkpoint Adaptation in Rhabdomyosarcoma
Článek How a Retrotransposon Exploits the Plant's Heat Stress Response for Its Activation
Článek A Nonsense Mutation in Encoding a Nondescript Transmembrane Protein Causes Idiopathic Male Subfertility in Cattle
Článek Deletion of a Conserved -Element in the Locus Highlights the Role of Acute Histone Acetylation in Modulating Inducible Gene Transcription
Článek Developmental Link between Sex and Nutrition; Regulates Sex-Specific Mandible Growth via Juvenile Hormone Signaling in Stag Beetles
Článek PP2A/B55 and Fcp1 Regulate Greatwall and Ensa Dephosphorylation during Mitotic Exit
Článek Differential Effects of Collagen Prolyl 3-Hydroxylation on Skeletal Tissues
Článek Comprehensive Functional Annotation of 77 Prostate Cancer Risk Loci
Článek Evolution of Chloroplast Transcript Processing in and Its Chromerid Algal Relatives
Článek A Chaperone-Assisted Degradation Pathway Targets Kinetochore Proteins to Ensure Genome Stability
Článek New MicroRNAs in —Birth, Death and Cycles of Adaptive Evolution
Článek A Genome-Wide Screen for Bacterial Envelope Biogenesis Mutants Identifies a Novel Factor Involved in Cell Wall Precursor Metabolism
Článek FGFR1-Frs2/3 Signalling Maintains Sensory Progenitors during Inner Ear Hair Cell Formation
Článek Regulation of Synaptic /Neuroligin Abundance by the /Nrf Stress Response Pathway Protects against Oxidative Stress
Článek Intrasubtype Reassortments Cause Adaptive Amino Acid Replacements in H3N2 Influenza Genes
Článek Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments
Článek WNT7B Promotes Bone Formation in part through mTORC1
Článek Natural Selection Reduced Diversity on Human Y Chromosomes
Článek In-Vivo Quantitative Proteomics Reveals a Key Contribution of Post-Transcriptional Mechanisms to the Circadian Regulation of Liver Metabolism
Článek The Candidate Splicing Factor Sfswap Regulates Growth and Patterning of Inner Ear Sensory Organs
Článek The Acid Phosphatase-Encoding Gene Contributes to Soybean Tolerance to Low-Phosphorus Stress
Článek p53 and TAp63 Promote Keratinocyte Proliferation and Differentiation in Breeding Tubercles of the Zebrafish
Článek Affects Plant Architecture by Regulating Local Auxin Biosynthesis
Článek The SET Domain Proteins SUVH2 and SUVH9 Are Required for Pol V Occupancy at RNA-Directed DNA Methylation Loci
Článek Down-Regulation of Rad51 Activity during Meiosis in Yeast Prevents Competition with Dmc1 for Repair of Double-Strand Breaks
Článek Multi-tissue Analysis of Co-expression Networks by Higher-Order Generalized Singular Value Decomposition Identifies Functionally Coherent Transcriptional Modules
Článek A Neurotoxic Glycerophosphocholine Impacts PtdIns-4, 5-Bisphosphate and TORC2 Signaling by Altering Ceramide Biosynthesis in Yeast
Článek Subtle Changes in Motif Positioning Cause Tissue-Specific Effects on Robustness of an Enhancer's Activity
Článek C/EBPα Is Required for Long-Term Self-Renewal and Lineage Priming of Hematopoietic Stem Cells and for the Maintenance of Epigenetic Configurations in Multipotent Progenitors
Článek The SPF27 Homologue Num1 Connects Splicing and Kinesin 1-Dependent Cytoplasmic Trafficking in
Článek Down-Regulation of eIF4GII by miR-520c-3p Represses Diffuse Large B Cell Lymphoma Development
Článek Genome Sequencing Highlights the Dynamic Early History of Dogs
Článek Re-sequencing Expands Our Understanding of the Phenotypic Impact of Variants at GWAS Loci
Článek Meta-Analysis Identifies Gene-by-Environment Interactions as Demonstrated in a Study of 4,965 Mice
Článek , a -Antisense Gene of , Encodes a Evolved Protein That Inhibits GSK3β Resulting in the Stabilization of MYCN in Human Neuroblastomas
Článek A Transcription Factor Is Wound-Induced at the Planarian Midline and Required for Anterior Pole Regeneration
Článek A Comprehensive tRNA Deletion Library Unravels the Genetic Architecture of the tRNA Pool
Článek A PNPase Dependent CRISPR System in
Článek Genomic Confirmation of Hybridisation and Recent Inbreeding in a Vector-Isolated Population
Článek Zinc Finger Transcription Factors Displaced SREBP Proteins as the Major Sterol Regulators during Saccharomycotina Evolution
Článek GATA6 Is a Crucial Regulator of Shh in the Limb Bud
Článek Tissue Specific Roles for the Ribosome Biogenesis Factor Wdr43 in Zebrafish Development
Článek A Cell Cycle and Nutritional Checkpoint Controlling Bacterial Surface Adhesion
Článek High Risk Population Isolate Reveals Low Frequency Variants Predisposing to Intracranial Aneurysms
Článek E3 Ubiquitin Ligase CHIP and NBR1-Mediated Selective Autophagy Protect Additively against Proteotoxicity in Plant Stress Responses
Článek Evolutionary Rate Covariation Identifies New Members of a Protein Network Required for Female Post-Mating Responses
Článek 3′ Untranslated Regions Mediate Transcriptional Interference between Convergent Genes Both Locally and Ectopically in
Článek Single Nucleus Genome Sequencing Reveals High Similarity among Nuclei of an Endomycorrhizal Fungus
Článek Metabolic QTL Analysis Links Chloroquine Resistance in to Impaired Hemoglobin Catabolism
Článek AL PHD-PRC1 Complexes Promote Seed Germination through H3K4me3-to-H3K27me3 Chromatin State Switch in Repression of Seed Developmental Genes
Článek Genomes Reveal Evolution of Microalgal Oleaginous Traits
Článek Large Inverted Duplications in the Human Genome Form via a Fold-Back Mechanism
Článek Variation in Genome-Wide Levels of Meiotic Recombination Is Established at the Onset of Prophase in Mammalian Males
Článek Age, Gender, and Cancer but Not Neurodegenerative and Cardiovascular Diseases Strongly Modulate Systemic Effect of the Apolipoprotein E4 Allele on Lifespan
Článek Lifespan Extension Conferred by Endoplasmic Reticulum Secretory Pathway Deficiency Requires Induction of the Unfolded Protein Response
Článek Is Non-Homologous End-Joining Really an Inherently Error-Prone Process?
Článek Vestigialization of an Allosteric Switch: Genetic and Structural Mechanisms for the Evolution of Constitutive Activity in a Steroid Hormone Receptor
Článek Functional Divergence and Evolutionary Turnover in Mammalian Phosphoproteomes
Článek A 660-Kb Deletion with Antagonistic Effects on Fertility and Milk Production Segregates at High Frequency in Nordic Red Cattle: Additional Evidence for the Common Occurrence of Balancing Selection in Livestock
Článek Comparative Evolutionary and Developmental Dynamics of the Cotton () Fiber Transcriptome
Článek The Transcription Factor BcLTF1 Regulates Virulence and Light Responses in the Necrotrophic Plant Pathogen
Článek Crossover Patterning by the Beam-Film Model: Analysis and Implications
Článek Single Cell Genomics: Advances and Future Perspectives
Článok vyšiel v časopise

PLOS Genetics

2014 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

nový kurz
Autori: doc. MUDr. David Zemánek, Ph.D., MUDr. Anna Chaloupka, Ph.D.
Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#