#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#
preLekára.sk / Odborné časopisy / PLOS Genetics / 2013 - 3

A Feed-Forward Loop Coupling Extracellular BMP Transport and Morphogenesis in Wing

English version České info

A variety of extracellular factors regulate morphogenesis during development. However, coordination between extracellular signaling and dynamic morphogenesis is largely unexplored. We address the fundamental question by studying posterior crossvein (PCV) development in Drosophila as a model, in which long-range BMP transport from the longitudinal veins plays a critical role during the pupal stages. Here, we show that RhoGAP Crossveinless-C (Cv-C) is induced at the PCV primordial cells by BMP signaling and mediates PCV morphogenesis cell-autonomously by inactivating members of the Rho-type small GTPases. Intriguingly, we find that Cv-C is also required non-cell-autonomously for BMP transport into the PCV region, while a long-range BMP transport is guided toward ectopic wing vein regions by loss of the Rho-type small GTPases. We present evidence that low level of ß-integrin accumulation at the basal side of PCV epithelial cells regulated by Cv-C provides an optimal extracellular environment for guiding BMP transport. These data suggest that BMP transport and PCV morphogenesis are tightly coupled. Our study reveals a feed-forward mechanism that coordinates the spatial distribution of extracellular instructive cues and morphogenesis. The coupling mechanism may be widely utilized to achieve precise morphogenesis during development and homeostasis.

Vyšlo v časopise: A Feed-Forward Loop Coupling Extracellular BMP Transport and Morphogenesis in Wing. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003403
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003403

Souhrn

A variety of extracellular factors regulate morphogenesis during development. However, coordination between extracellular signaling and dynamic morphogenesis is largely unexplored. We address the fundamental question by studying posterior crossvein (PCV) development in Drosophila as a model, in which long-range BMP transport from the longitudinal veins plays a critical role during the pupal stages. Here, we show that RhoGAP Crossveinless-C (Cv-C) is induced at the PCV primordial cells by BMP signaling and mediates PCV morphogenesis cell-autonomously by inactivating members of the Rho-type small GTPases. Intriguingly, we find that Cv-C is also required non-cell-autonomously for BMP transport into the PCV region, while a long-range BMP transport is guided toward ectopic wing vein regions by loss of the Rho-type small GTPases. We present evidence that low level of ß-integrin accumulation at the basal side of PCV epithelial cells regulated by Cv-C provides an optimal extracellular environment for guiding BMP transport. These data suggest that BMP transport and PCV morphogenesis are tightly coupled. Our study reveals a feed-forward mechanism that coordinates the spatial distribution of extracellular instructive cues and morphogenesis. The coupling mechanism may be widely utilized to achieve precise morphogenesis during development and homeostasis.

Zdroje

1. AffolterM, BaslerK (2007) The Decapentaplegic morphogen gradient: from pattern formation to growth regulation. Nat Rev Genet 8 : 663–674.

2. WuMY, HillCS (2009) Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev Cell 16 : 329–343.

3. ParkerL, StathakisDG, AroraK (2004) Regulation of BMP and activin signaling in Drosophila. Prog Mol Subcell Biol 34 : 73–101.

4. JaffeAB, HallA (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21 : 247–269.

5. SchwartzMA, ShattilSJ (2000) Signaling networks linking integrins and rho family GTPases. Trends Biochem Sci 25 : 388–391.

6. RossmanKL, DerCJ, SondekJ (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 6 : 167–180.

7. MoonSY, ZhengY (2003) Rho GTPase-activating proteins in cell regulation. Trends Cell Biol 13 : 13–22.

8. CorderoJB, LarsonDE, CraigCR, HaysR, CaganR (2007) Dynamic decapentaplegic signaling regulates patterning and adhesion in the Drosophila pupal retina. Development 134 : 1861–1871.

9. WidmannTJ, DahmannC (2009) Dpp signaling promotes the cuboidal-to-columnar shape transition of Drosophila wing disc epithelia by regulating Rho1. J Cell Sci 122 : 1362–1373.

10. RalstonA, BlairSS (2005) Long-range Dpp signaling is regulated to restrict BMP signaling to a crossvein competent zone. Dev Biol 280 : 187–200.

11. ShimmiO, RalstonA, BlairSS, O'ConnorMB (2005) The crossveinless gene encodes a new member of the Twisted gastrulation family of BMP-binding proteins which, with Short gastrulation, promotes BMP signaling in the crossveins of the Drosophila wing. Dev Biol 282 : 70–83.

12. SerpeM, RalstonA, BlairSS, O'ConnorMB (2005) Matching catalytic activity to developmental function: tolloid-related processes Sog in order to help specify the posterior crossvein in the Drosophila wing. Development 132 : 2645–2656.

13. MatsudaS, ShimmiO (2012) Directional transport and active retention of Dpp/BMP create wing vein patterns in Drosophila. Dev Biol 366 : 153–162.

14. ShimmiO, UmulisD, OthmerH, O'ConnorMB (2005) Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm embryo. Cell 120 : 873–886.

15. WangYC, FergusonEL (2005) Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 434 : 229–234.

16. O'ConnorMB, UmulisD, OthmerHG, BlairSS (2006) Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133 : 183–193.

17. HoganBL, KolodziejPA (2002) Organogenesis: molecular mechanisms of tubulogenesis. Nat Rev Genet 3 : 513–523.

18. SternC (1934) On the Occurrence of Translocations and Autosomal Non-Disjunction in Drosophila melanogaster. Proc Natl Acad Sci U S A 20 : 36–39.

19. DenholmB, BrownS, RayRP, Ruiz-GomezM, SkaerH, et al. (2005) crossveinless-c is a RhoGAP required for actin reorganisation during morphogenesis. Development 132 : 2389–2400.

20. FristromD, WilcoxM, FristromJ (1993) The distribution of PS integrins, laminin A and F-actin during key stages in Drosophila wing development. Development 117 : 509–523.

21. St JohnstonRD, HoffmannFM, BlackmanRK, SegalD, GrimailaR, et al. (1990) Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev 4 : 1114–1127.

22. BroduV, CasanovaJ (2006) The RhoGAP crossveinless-c links trachealess and EGFR signaling to cell shape remodeling in Drosophila tracheal invagination. Genes Dev 20 : 1817–1828.

23. SimoesS, DenholmB, AzevedoD, SotillosS, MartinP, et al. (2006) Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis. Development 133 : 4257–4267.

24. FehonRG, OrenT, LaJeunesseDR, MelbyTE, McCartneyBM (1997) Isolation of mutations in the Drosophila homologues of the human Neurofibromatosis 2 and yeast CDC42 genes using a simple and efficient reverse-genetic method. Genetics 146 : 245–252.

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

26. SerpeM, UmulisD, RalstonA, ChenJ, OlsonDJ, et al. (2008) The BMP-binding protein Crossveinless 2 is a short-range, concentration-dependent, biphasic modulator of BMP signaling in Drosophila. Dev Cell 14 : 940–953.

27. TelemanAA, CohenSM (2000) Dpp gradient formation in the Drosophila wing imaginal disc. Cell 103 : 971–980.

28. BaronM, O'LearyV, EvansDA, HicksM, HudsonK (2000) Multiple roles of the Dcdc42 GTPase during wing development in Drosophila melanogaster. Mol Gen Genet 264 : 98–104.

29. GenovaJL, JongS, CampJT, FehonRG (2000) Functional analysis of Cdc42 in actin filament assembly, epithelial morphogenesis, and cell signaling during Drosophila development. Dev Biol 221 : 181–194.

30. AraujoH, NegreirosE, BierE (2003) Integrins modulate Sog activity in the Drosophila wing. Development 130 : 3851–3864.

31. WilcoxM, DiAntonioA, LeptinM (1989) The function of PS integrins in Drosophila wing morphogenesis. Development 107 : 891–897.

32. BementWM, MillerAL, von DassowG (2006) Rho GTPase activity zones and transient contractile arrays. Bioessays 28 : 983–993.

33. YanJ, LuQ, FangX, AdlerPN (2009) Rho1 has multiple functions in Drosophila wing planar polarity. Dev Biol 333 : 186–199.

34. Dominguez-GimenezP, BrownNH, Martin-BermudoMD (2007) Integrin-ECM interactions regulate the changes in cell shape driving the morphogenesis of the Drosophila wing epithelium. J Cell Sci 120 : 1061–1071.

35. ChenJ, HoneyagerSM, SchleedeJ, AvanesovA, LaughonA, et al. (2012) Crossveinless d is a vitellogenin-like lipoprotein that binds BMPs and HSPGs, and is required for normal BMP signaling in the Drosophila wing. Development 139 : 2170–2176.

36. BuntS, HooleyC, HuN, ScahillC, WeaversH, et al. (2010) Hemocyte-secreted type IV collagen enhances BMP signaling to guide renal tubule morphogenesis in Drosophila. Dev Cell 19 : 296–306.

37. WangX, HarrisRE, BaystonLJ, AsheHL (2008) Type IV collagens regulate BMP signalling in Drosophila. Nature 455 : 72–77.

38. Pastor-ParejaJC, XuT (2011) Shaping cells and organs in Drosophila by opposing roles of fat body-secreted Collagen IV and perlecan. Dev Cell 21 : 245–256.

39. MurrayMA, FesslerLI, PalkaJ (1995) Changing distributions of extracellular matrix components during early wing morphogenesis in Drosophila. Dev Biol 168 : 150–165.

40. VuilleumierR, SpringhornA, PattersonL, KoidlS, HammerschmidtM, et al. (2010) Control of Dpp morphogen signalling by a secreted feedback regulator. Nat Cell Biol 12 : 611–617.

41. SzuperakM, SalahS, MeyerEJ, NagarajanU, IkmiA, et al. (2011) Feedback regulation of Drosophila BMP signaling by the novel extracellular protein larval translucida. Development 138 : 715–724.

42. KesavanG, SandFW, GreinerTU, JohanssonJK, KobberupS, et al. (2009) Cdc42-mediated tubulogenesis controls cell specification. Cell 139 : 791–801.

43. LahozA, HallA (2008) DLC1: a significant GAP in the cancer genome. Genes Dev 22 : 1724–1730.

44. MassagueJ (2008) TGFbeta in Cancer. Cell 134 : 215–230.

Štítky
Genetika Reprodukčná medicína
Článek Power and Predictive Accuracy of Polygenic Risk Scores
Článek Rare Copy Number Variants Are a Common Cause of Short Stature
Článek Coordination of Flower Maturation by a Regulatory Circuit of Three MicroRNAs
Článek Ubiquitous Polygenicity of Human Complex Traits: Genome-Wide Analysis of 49 Traits in Koreans
Článek Genomic Evidence for Island Population Conversion Resolves Conflicting Theories of Polar Bear Evolution
Článek Mechanistic Insight into the Pathology of Polyalanine Expansion Disorders Revealed by a Mouse Model for X Linked Hypopituitarism
Článek Genome-Wide Association Study and Gene Expression Analysis Identifies as a Predictor of Response to Etanercept Therapy in Rheumatoid Arthritis
Článek Problem Solved: An Interview with Sir Edwin Southern
Článek Long Interspersed Element–1 (LINE-1): Passenger or Driver in Human Neoplasms?
Článek Mouse HFM1/Mer3 Is Required for Crossover Formation and Complete Synapsis of Homologous Chromosomes during Meiosis
Článek Alternative Splicing and Subfunctionalization Generates Functional Diversity in Fungal Proteomes
Článek A WRKY Transcription Factor Recruits the SYG1-Like Protein SHB1 to Activate Gene Expression and Seed Cavity Enlargement
Článek Microhomology-Mediated Mechanisms Underlie Non-Recurrent Disease-Causing Microdeletions of the Gene or Its Regulatory Domain
Článek Ancient Evolutionary Trade-Offs between Yeast Ploidy States
Článek Differential Evolutionary Fate of an Ancestral Primate Endogenous Retrovirus Envelope Gene, the EnvV , Captured for a Function in Placentation
Článek The Tomato Yellow Leaf Curl Virus Resistance Genes and Are Allelic and Code for DFDGD-Class RNA–Dependent RNA Polymerases
Článek The U-Box E3 Ubiquitin Ligase TUD1 Functions with a Heterotrimeric G α Subunit to Regulate Brassinosteroid-Mediated Growth in Rice
Článek Role of the DSC1 Channel in Regulating Neuronal Excitability in : Extending Nervous System Stability under Stress
Článek –Independent Phenotypic Switching in and a Dual Role for Wor1 in Regulating Switching and Filamentation
Článek Pax6 Regulates Gene Expression in the Vertebrate Lens through miR-204
Článek Blood-Informative Transcripts Define Nine Common Axes of Peripheral Blood Gene Expression
Článek Genetic Architecture of Skin and Eye Color in an African-European Admixed Population
Článek Fine Characterisation of a Recombination Hotspot at the Locus and Resolution of the Paradoxical Excess of Duplications over Deletions in the General Population
Článek Estrogen Mediated-Activation of miR-191/425 Cluster Modulates Tumorigenicity of Breast Cancer Cells Depending on Estrogen Receptor Status
Článek Complex Patterns of Genomic Admixture within Southern Africa
Článek Yap- and Cdc42-Dependent Nephrogenesis and Morphogenesis during Mouse Kidney Development
Článek Molecular Networks of Human Muscle Adaptation to Exercise and Age
Článek Alp/Enigma Family Proteins Cooperate in Z-Disc Formation and Myofibril Assembly
Článek Polycomb Group Gene Regulates Rice () Seed Development and Grain Filling via a Mechanism Distinct from
Článek RFX Transcription Factor DAF-19 Regulates 5-HT and Innate Immune Responses to Pathogenic Bacteria in
Článek Distinct Molecular Strategies for Hox-Mediated Limb Suppression in : From Cooperativity to Dispensability/Antagonism in TALE Partnership
Článek A Natural Polymorphism in rDNA Replication Origins Links Origin Activation with Calorie Restriction and Lifespan
Článek TDP2–Dependent Non-Homologous End-Joining Protects against Topoisomerase II–Induced DNA Breaks and Genome Instability in Cells and
Článek Recurrent Rearrangement during Adaptive Evolution in an Interspecific Yeast Hybrid Suggests a Model for Rapid Introgression
Článek Genome-Wide Association Study in Mutation Carriers Identifies Novel Loci Associated with Breast and Ovarian Cancer Risk
Článek Coincident Resection at Both Ends of Random, γ–Induced Double-Strand Breaks Requires MRX (MRN), Sae2 (Ctp1), and Mre11-Nuclease
Článek Identification of a -Specific Modifier Locus at 6p24 Related to Breast Cancer Risk
Článek A Novel Function for the Hox Gene in the Male Accessory Gland Regulates the Long-Term Female Post-Mating Response in
Článek Tdp2: A Means to Fixing the Ends
Článek A Novel Role for the RNA–Binding Protein FXR1P in Myoblasts Cell-Cycle Progression by Modulating mRNA Stability
Článek Association Mapping and the Genomic Consequences of Selection in Sunflower
Článek Histone Deacetylase 2 (HDAC2) Regulates Chromosome Segregation and Kinetochore Function via H4K16 Deacetylation during Oocyte Maturation in Mouse
Článek A Novel Mutation in the Upstream Open Reading Frame of the Gene Causes a MEN4 Phenotype
Článek Ataxin1L Is a Regulator of HSC Function Highlighting the Utility of Cross-Tissue Comparisons for Gene Discovery
Článek Human Spermatogenic Failure Purges Deleterious Mutation Load from the Autosomes and Both Sex Chromosomes, including the Gene
Článek A Conserved Upstream Motif Orchestrates Autonomous, Germline-Enriched Expression of piRNAs
Článek Statistical Analysis Reveals Co-Expression Patterns of Many Pairs of Genes in Yeast Are Jointly Regulated by Interacting Loci
Článek Matefin/SUN-1 Phosphorylation Is Part of a Surveillance Mechanism to Coordinate Chromosome Synapsis and Recombination with Meiotic Progression and Chromosome Movement
Článek A Role for the Malignant Brain Tumour (MBT) Domain Protein LIN-61 in DNA Double-Strand Break Repair by Homologous Recombination
Článek The Population and Evolutionary Dynamics of Phage and Bacteria with CRISPR–Mediated Immunity
Článek Long Noncoding RNA MALAT1 Controls Cell Cycle Progression by Regulating the Expression of Oncogenic Transcription Factor B-MYB
Článek Surveillance-Activated Defenses Block the ROS–Induced Mitochondrial Unfolded Protein Response
Článek DNA Topoisomerase III Localizes to Centromeres and Affects Centromeric CENP-A Levels in Fission Yeast
Článek Genome-Wide Control of RNA Polymerase II Activity by Cohesin
Článek Divergent Selection Drives Genetic Differentiation in an R2R3-MYB Transcription Factor That Contributes to Incipient Speciation in
Článek NODULE INCEPTION Directly Targets Subunit Genes to Regulate Essential Processes of Root Nodule Development in
Článek Spreading of a Prion Domain from Cell-to-Cell by Vesicular Transport in
Článek Deficiency in Origin Licensing Proteins Impairs Cilia Formation: Implications for the Aetiology of Meier-Gorlin Syndrome
Článek Deficiency Reduces Adipose OXPHOS Capacity and Triggers Inflammation and Insulin Resistance in Mice
Článek The Conserved SKN-1/Nrf2 Stress Response Pathway Regulates Synaptic Function in
Článek Functional Genomic Analysis of the Regulatory Network in
Článek Astakine 2—the Dark Knight Linking Melatonin to Circadian Regulation in Crustaceans
Článek CRL2 E3-Ligase Regulates Proliferation and Progression through Meiosis in the Germline
Článek Both the Caspase CSP-1 and a Caspase-Independent Pathway Promote Programmed Cell Death in Parallel to the Canonical Pathway for Apoptosis in
Článek PRMT4 Is a Novel Coactivator of c-Myb-Dependent Transcription in Haematopoietic Cell Lines
Článek A Copy Number Variant at the Locus Likely Confers Risk for Canine Squamous Cell Carcinoma of the Digit
Článek Evidence of Gene–Environment Interactions between Common Breast Cancer Susceptibility Loci and Established Environmental Risk Factors
Článek HIV Infection Disrupts the Sympatric Host–Pathogen Relationship in Human Tuberculosis
Článek Trans-Ethnic Fine-Mapping of Lipid Loci Identifies Population-Specific Signals and Allelic Heterogeneity That Increases the Trait Variance Explained
Článek A Gene Transfer Agent and a Dynamic Repertoire of Secretion Systems Hold the Keys to the Explosive Radiation of the Emerging Pathogen
Článek The Role of ATM in the Deficiency in Nonhomologous End-Joining near Telomeres in a Human Cancer Cell Line
Článek Dynamic Circadian Protein–Protein Interaction Networks Predict Temporal Organization of Cellular Functions
Článek Nuclear Myosin 1c Facilitates the Chromatin Modifications Required to Activate rRNA Gene Transcription and Cell Cycle Progression
Článek Robust Prediction of Expression Differences among Human Individuals Using Only Genotype Information
Článek A Single Cohesin Complex Performs Mitotic and Meiotic Functions in the Protist
Článek The Role of the Arabidopsis Exosome in siRNA–Independent Silencing of Heterochromatic Loci
Článek Elevated Expression of the Integrin-Associated Protein PINCH Suppresses the Defects of Muscle Hypercontraction Mutants
Článek Twist1 Controls a Cell-Specification Switch Governing Cell Fate Decisions within the Cardiac Neural Crest
Článek Genome-Wide Testing of Putative Functional Exonic Variants in Relationship with Breast and Prostate Cancer Risk in a Multiethnic Population
Článek Heteroduplex DNA Position Defines the Roles of the Sgs1, Srs2, and Mph1 Helicases in Promoting Distinct Recombination Outcomes
Článok vyšiel v časopise

PLOS Genetics

2013 Číslo 3
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#