-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
DAAM Is Required for Thin Filament Formation and Sarcomerogenesis during Muscle Development in Drosophila
During muscle development, myosin and actin containing filaments assemble into the highly organized sarcomeric structure critical for muscle function. Although sarcomerogenesis clearly involves the de novo formation of actin filaments, this process remained poorly understood. Here we show that mouse and Drosophila members of the DAAM formin family are sarcomere-associated actin assembly factors enriched at the Z-disc and M-band. Analysis of dDAAM mutants revealed a pivotal role in myofibrillogenesis of larval somatic muscles, indirect flight muscles and the heart. We found that loss of dDAAM function results in multiple defects in sarcomere development including thin and thick filament disorganization, Z-disc and M-band formation, and a near complete absence of the myofibrillar lattice. Collectively, our data suggest that dDAAM is required for the initial assembly of thin filaments, and subsequently it promotes filament elongation by assembling short actin polymers that anneal to the pointed end of the growing filaments, and by antagonizing the capping protein Tropomodulin.
Vyšlo v časopise: DAAM Is Required for Thin Filament Formation and Sarcomerogenesis during Muscle Development in Drosophila. PLoS Genet 10(2): e32767. doi:10.1371/journal.pgen.1004166
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004166Souhrn
During muscle development, myosin and actin containing filaments assemble into the highly organized sarcomeric structure critical for muscle function. Although sarcomerogenesis clearly involves the de novo formation of actin filaments, this process remained poorly understood. Here we show that mouse and Drosophila members of the DAAM formin family are sarcomere-associated actin assembly factors enriched at the Z-disc and M-band. Analysis of dDAAM mutants revealed a pivotal role in myofibrillogenesis of larval somatic muscles, indirect flight muscles and the heart. We found that loss of dDAAM function results in multiple defects in sarcomere development including thin and thick filament disorganization, Z-disc and M-band formation, and a near complete absence of the myofibrillar lattice. Collectively, our data suggest that dDAAM is required for the initial assembly of thin filaments, and subsequently it promotes filament elongation by assembling short actin polymers that anneal to the pointed end of the growing filaments, and by antagonizing the capping protein Tropomodulin.
Zdroje
1. LutherPK (2009) The vertebrate muscle Z-disc: sarcomere anchor for structure and signalling. J Muscle Res Cell Motil 30 : 171–185.
2. SparrowJC, SchockF (2009) The initial steps of myofibril assembly: integrins pave the way. Nat Rev Mol Cell Biol 10 : 293–298.
3. PollardTD, BlanchoinL, MullinsRD (2000) Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29 : 545–576.
4. CampelloneKG, WelchMD (2010) A nucleator arms race: cellular control of actin assembly. Nat Rev Mol Cell Biol 11 : 237–251.
5. ChesaroneM, GouldCJ, MoseleyJB, GoodeBL (2009) Displacement of formins from growing barbed ends by bud14 is critical for actin cable architecture and function. Dev Cell 16 : 292–302.
6. ChereauD, BoczkowskaM, Skwarek-MaruszewskaA, FujiwaraI, HayesDB, et al. (2008) Leiomodin is an actin filament nucleator in muscle cells. Science 320 : 239–243.
7. TaniguchiK, TakeyaR, SuetsuguS, KanOM, NarusawaM, et al. (2009) Mammalian formin fhod3 regulates actin assembly and sarcomere organization in striated muscles. J Biol Chem 284 : 29873–29881.
8. Skwarek-MaruszewskaA, BoczkowskaM, ZajacAL, KremnevaE, SvitkinaT, et al. (2010) Different localizations and cellular behaviors of leiomodin and tropomodulin in mature cardiomyocyte sarcomeres. Mol Biol Cell 21 : 3352–3361.
9. TsukadaT, PappasCT, MorozN, AntinPB, KostyukovaAS, et al. (2010) Leiomodin-2 is an antagonist of tropomodulin-1 at the pointed end of the thin filaments in cardiac muscle. J Cell Sci 123 : 3136–3145.
10. IskratschT, LangeS, DwyerJ, KhoAL, dos RemediosC, et al. (2010) Formin follows function: a muscle-specific isoform of FHOD3 is regulated by CK2 phosphorylation and promotes myofibril maintenance. Journal of Cell Biology 191 : 1159–1172.
11. IskratschT, ReijntjesS, DwyerJ, ToselliP, DeganoIR, et al. (2013) Two distinct phosphorylation events govern the function of muscle FHOD3. Cell Mol Life Sci 70 : 893–908.
12. AnheziniL, SaitaAP, CostaMS, RamosRG, SimonCR (2012) Fhos encodes a Drosophila Formin-like protein participating in autophagic programmed cell death. Genesis 50 : 672–684.
13. CastrillonDH, WassermanSA (1994) Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120 : 3367–3377.
14. EmmonsS, PhanH, CalleyJ, ChenW, JamesB, et al. (1995) Cappuccino, a Drosophila maternal effect gene required for polarity of the egg and embryo, is related to the vertebrate limb deformity locus. Genes Dev 9 : 2482–2494.
15. TanakaH, TakasuE, AigakiT, KatoK, HayashiS, et al. (2004) Formin3 is required for assembly of the F-actin structure that mediates tracheal fusion in Drosophila. Dev Biol 274 : 413–425.
16. LittlefieldRS, FowlerVM (2008) Thin filament length regulation in striated muscle sarcomeres: pointed-end dynamics go beyond a nebulin ruler. Semin Cell Dev Biol 19 : 511–519.
17. LittlefieldR, Almenar-QueraltA, FowlerVM (2001) Actin dynamics at pointed ends regulates thin filament length in striated muscle. Nat Cell Biol 3 : 544–551.
18. BaiJ, HartwigJH, PerrimonN (2007) SALS, a WH2-domain-containing protein, promotes sarcomeric actin filament elongation from pointed ends during Drosophila muscle growth. Dev Cell 13 : 828–842.
19. KatzemichA, KreiskotherN, AlexandrovichA, ElliottC, SchockF, et al. (2012) The function of the M-line protein obscurin in controlling the symmetry of the sarcomere in the flight muscle of Drosophila. J Cell Sci 125 : 3367–3379.
20. ReedyMC, BeallC (1993) Ultrastructure of developing flight muscle in Drosophila. I. Assembly of myofibrils. Dev Biol 160 : 443–465.
21. XuY, MoseleyJB, SagotI, PoyF, PellmanD, et al. (2004) Crystal structures of a Formin Homology-2 domain reveal a tethered dimer architecture. Cell 116 : 711–723.
22. MatusekT, DjianeA, JankovicsF, BrunnerD, MlodzikM, et al. (2006) The Drosophila formin DAAM regulates the tracheal cuticle pattern through organizing the actin cytoskeleton. Development 133 : 957–966.
23. LiDQ, HallettMA, ZhuWQ, RubartM, LiuY, et al. (2011) Dishevelled-associated activator of morphogenesis 1 (Daam1) is required for heart morphogenesis. Development 138 : 303–315.
24. YaffeD, SaxelO (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270 : 725–727.
25. Kontrogianni-KonstantopoulosA, CatinoDH, StrongJC, BlochRJ (2006) De novo myofibrillogenesis in C2C12 cells: evidence for the independent assembly of M bands and Z disks. Am J Physiol Cell Physiol 290: C626–637.
26. TrombitasK, GreaserM, FrenchG, GranzierH (1998) PEVK extension of human soleus muscle titin revealed by immunolabeling with the anti-titin antibody 9D10. J Struct Biol 122 : 188–196.
27. WangSM, GreaserML, SchultzE, BulinskiJC, LinJJ, et al. (1988) Studies on cardiac myofibrillogenesis with antibodies to titin, actin, tropomyosin, and myosin. J Cell Biol 107 : 1075–1083.
28. GroveBK, KurerV, LehnerC, DoetschmanTC, PerriardJC, et al. (1984) A new 185,000-dalton skeletal muscle protein detected by monoclonal antibodies. J Cell Biol 98 : 518–524.
29. KarlikCC, FyrbergEA (1985) An insertion within a variably spliced Drosophila tropomyosin gene blocks accumulation of only one encoded isoform. Cell 41 : 57–66.
30. OkamotoH, HiromiY, IshikawaE, YamadaT, IsodaK, et al. (1986) Molecular characterization of mutant actin genes which induce heat-shock proteins in Drosophila flight muscles. EMBO J 5 : 589–596.
31. FyrbergEA, MahaffeyJW, BondBJ, DavidsonN (1983) Transcripts of the six Drosophila actin genes accumulate in a stage - and tissue-specific manner. Cell 33 : 115–123.
32. TetzlaffMT, JackleH, PankratzMJ (1996) Lack of Drosophila cytoskeletal tropomyosin affects head morphogenesis and the accumulation of oskar mRNA required for germ cell formation. EMBO J 15 : 1247–1254.
33. BarkoS, BugyiB, CarlierMF, GombosR, MatusekT, et al. (2010) Characterization of the biochemical properties and biological function of the formin homology domains of Drosophila DAAM. J Biol Chem 285 : 13154–13169.
34. Fritz-SixKL, CoxPR, FischerRS, XuB, GregorioCC, et al. (2003) Aberrant myofibril assembly in tropomodulin1 null mice leads to aborted heart development and embryonic lethality. J Cell Biol 163 : 1033–1044.
35. McKeownCR, NowakRB, MoyerJ, SussmanMA, FowlerVM (2008) Tropomodulin1 is required in the heart but not the yolk sac for mouse embryonic development. Circ Res 103 : 1241–1248.
36. StevensonTO, MercerKB, CoxEA, SzewczykNJ, ConleyCA, et al. (2007) unc-94 encodes a tropomodulin in Caenorhabditis elegans. J Mol Biol 374 : 936–950.
37. YamashiroS, CoxEA, BaillieDL, HardinJD, OnoS (2008) Sarcomeric actin organization is synergistically promoted by tropomodulin, ADF/cofilin, AIP1 and profilin in C. elegans. J Cell Sci 121 : 3867–3877.
38. SussmanMA, BaqueS, UhmCS, DanielsMP, PriceRL, et al. (1998) Altered expression of tropomodulin in cardiomyocytes disrupts the sarcomeric structure of myofibrils. Circ Res 82 : 94–105.
39. LuJ, MengW, PoyF, MaitiS, GoodeBL, et al. (2007) Structure of the FH2 domain of Daam1: implications for formin regulation of actin assembly. J Mol Biol 369 : 1258–1269.
40. ShimadaA, NyitraiM, VetterIR, KuhlmannD, BugyiB, et al. (2004) The core FH2 domain of diaphanous-related formins is an elongated actin binding protein that inhibits polymerization. Mol Cell 13 : 511–522.
41. AndrianantoandroE, BlanchoinL, SeptD, McCammonJA, PollardTD (2001) Kinetic mechanism of end-to-end annealing of actin filaments. J Mol Biol 312 : 721–730.
42. SkauCT, NeidtEM, KovarDR (2009) Role of tropomyosin in formin-mediated contractile ring assembly in fission yeast. Mol Biol Cell 20 : 2160–2173.
43. Mardahl-DumesnilM, FowlerVM (2001) Thin filaments elongate from their pointed ends during myofibril assembly in Drosophila indirect flight muscle. J Cell Biol 155 : 1043–1053.
44. Mi-MiL, VotraS, KemphuesK, BretscherA, PruyneD (2012) Z-line formins promote contractile lattice growth and maintenance in striated muscles of C. elegans. J Cell Biol 198 : 87–102.
45. NakayaMA, HabasR, BirisK, DuntyWCJr, KatoY, et al. (2004) Identification and comparative expression analyses of Daam genes in mouse and Xenopus. Gene Expr Patterns 5 : 97–105.
46. KanOM, TakeyaR, AbeT, KitajimaN, NishidaM, et al. (2012) Mammalian formin Fhod3 plays an essential role in cardiogenesis by organizing myofibrillogenesis. Biol Open 1 : 889–896.
47. Kan-oM, TakeyaR, TaniguchiK, TanoueY, TominagaR, et al. (2012) Expression and subcellular localization of mammalian formin Fhod3 in the embryonic and adult heart. PLoS One 7: e34765.
48. BeallCJ, SepanskiMA, FyrbergEA (1989) Genetic dissection of Drosophila myofibril formation: effects of actin and myosin heavy chain null alleles. Genes Dev 3 : 131–140.
49. RoperK, MaoY, BrownNH (2005) Contribution of sequence variation in Drosophila actins to their incorporation into actin-based structures in vivo. J Cell Sci 118 : 3937–3948.
50. MatusekT, GombosR, SzecsenyiA, Sanchez-SorianoN, CzibulaA, et al. (2008) Formin proteins of the DAAM subfamily play a role during axon growth. J Neurosci 28 : 13310–13319.
51. MogamiK, HottaY (1981) Isolation of Drosophila flightless mutants which affect myofibrillar proteins of indirect flight muscle. Mol Gen Genet 183 : 409–417.
52. MorinX, DanemanR, ZavortinkM, ChiaW (2001) A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc Natl Acad Sci U S A 98 : 15050–15055.
53. AlayariNN, VoglerG, Taghli-LamallemO, OcorrK, BodmerR, et al. (2009) Fluorescent labeling of Drosophila heart structures. J Vis Exp (32) pii: 1423.
54. CrippsRM, BallE, StarkM, LawnA, SparrowJC (1994) Recovery of dominant, autosomal flightless mutants of Drosophila melanogaster and identification of a new gene required for normal muscle structure and function. Genetics 137 : 151–164.
55. VinckierA, SemenzaG (1998) Measuring elasticity of biological materials by atomic force microscopy. FEBS Lett 430 : 12–16.
Štítky
Genetika Reprodukčná medicína
Článek Natural Polymorphisms in Influence Negative Selection and CD4∶CD8 Lineage Commitment in the RatČlánek MicroRNAs Located in the Hox Gene Clusters Are Implicated in Huntington's Disease PathogenesisČlánek Comparative RNAi Screens in and Reveal the Impact of Developmental System Drift on Gene FunctionČlánek Mutation of SLC35D3 Causes Metabolic Syndrome by Impairing Dopamine Signaling in Striatal D1 Neurons
Článok vyšiel v časopisePLOS Genetics
Najčítanejšie tento týždeň
2014 Číslo 2- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
-
Všetky články tohto čísla
- Fifteen Years Later: Hard and Soft Selection Sweeps Confirm a Large Population Number for HIV In Vivo
- The Same but Different: Worms Reveal the Pervasiveness of Developmental System Drift
- Serine Carboxypeptidase SCPEP1 and Cathepsin A Play Complementary Roles in Regulation of Vasoconstriction via Inactivation of Endothelin-1
- Coherent Functional Modules Improve Transcription Factor Target Identification, Cooperativity Prediction, and Disease Association
- A Long-Chain Flavodoxin Protects from Oxidative Stress and Host Bacterial Clearance
- Mammalian E-type Cyclins Control Chromosome Pairing, Telomere Stability and CDK2 Localization in Male Meiosis
- Influenza Virus Drug Resistance: A Time-Sampled Population Genetics Perspective
- Transcriptome-Wide Analyses of 5′-Ends in RNase J Mutants of a Gram-Positive Pathogen Reveal a Role in RNA Maturation, Regulation and Degradation
- Selective Disruption of Aurora C Kinase Reveals Distinct Functions from Aurora B Kinase during Meiosis in Mouse Oocytes
- X Chromosome Control of Meiotic Chromosome Synapsis in Mouse Inter-Subspecific Hybrids
- A Cohesin-Independent Role for NIPBL at Promoters Provides Insights in CdLS
- Extreme Population Differences in the Human Zinc Transporter ZIP4 (SLC39A4) Are Explained by Positive Selection in Sub-Saharan Africa
- Classic Selective Sweeps Revealed by Massive Sequencing in Cattle
- Genomic Networks of Hybrid Sterility
- Natural Polymorphisms in Influence Negative Selection and CD4∶CD8 Lineage Commitment in the Rat
- Oxidative Stress Is Not a Major Contributor to Somatic Mitochondrial DNA Mutations
- Molecular Identification of Collagen 17a1 as a Major Genetic Modifier of Laminin Gamma 2 Mutation-Induced Junctional Epidermolysis Bullosa in Mice
- Uncoupling of Molecular Maturation from Peripheral Target Innervation in Nociceptors Expressing a Chimeric TrkA/TrkC Receptor
- MicroRNAs Located in the Hox Gene Clusters Are Implicated in Huntington's Disease Pathogenesis
- Loss of Trabid, a New Negative Regulator of the Immune-Deficiency Pathway at the Level of TAK1, Reduces Life Span
- Targeted Ablation of Nesprin 1 and Nesprin 2 from Murine Myocardium Results in Cardiomyopathy, Altered Nuclear Morphology and Inhibition of the Biomechanical Gene Response
- Identification of Novel Genetic Loci Associated with Thyroid Peroxidase Antibodies and Clinical Thyroid Disease
- CEP-1, the p53 Homolog, Mediates Opposing Longevity Outcomes in Mitochondrial Electron Transport Chain Mutants
- Transcriptomics and Functional Genomics of ROS-Induced Cell Death Regulation by
- Quantitative Genome-Wide Genetic Interaction Screens Reveal Global Epistatic Relationships of Protein Complexes in
- Cascades of Genetic Instability Resulting from Compromised Break-Induced Replication
- Serine- and Threonine/Valine-Dependent Activation of PDK and Tor Orthologs Converge on Sch9 to Promote Aging
- Zfp322a Regulates Mouse ES Cell Pluripotency and Enhances Reprogramming Efficiency
- Insertional Mutagenesis and Deep Profiling Reveals Gene Hierarchies and a -Dependent Bottleneck in Lymphomagenesis
- DAAM Is Required for Thin Filament Formation and Sarcomerogenesis during Muscle Development in Drosophila
- Plasma Cholesterol–Induced Lesion Networks Activated before Regression of Early, Mature, and Advanced Atherosclerosis
- High-Resolution Profiling of Stationary-Phase Survival Reveals Yeast Longevity Factors and Their Genetic Interactions
- Comparative RNAi Screens in and Reveal the Impact of Developmental System Drift on Gene Function
- Accurate and Robust Genomic Prediction of Celiac Disease Using Statistical Learning
- Sex-Specific Embryonic Gene Expression in Species with Newly Evolved Sex Chromosomes
- Chromosome X-Wide Association Study Identifies Loci for Fasting Insulin and Height and Evidence for Incomplete Dosage Compensation
- Negative Feedback and Transcriptional Overshooting in a Regulatory Network for Horizontal Gene Transfer
- DNA Sequence Explains Seemingly Disordered Methylation Levels in Partially Methylated Domains of Mammalian Genomes
- Insights into the Genomic Landscape: Comparative Genomics Reveals Variations in Ploidy and Nutrient Utilisation Potential amongst Wine Isolates
- Molecular Evidence for the Inverse Comorbidity between Central Nervous System Disorders and Cancers Detected by Transcriptomic Meta-analyses
- The Centriolar Satellite Protein AZI1 Interacts with BBS4 and Regulates Ciliary Trafficking of the BBSome
- Fine-Mapping the Region Detects Common Variants Tagging a Rare Coding Allele: Evidence for Synthetic Association in Prostate Cancer
- Transmission Distortion Affecting Human Noncrossover but Not Crossover Recombination: A Hidden Source of Meiotic Drive
- A Variant in the Neuropeptide Receptor is a Major Determinant of Growth and Physiology
- Mutation of SLC35D3 Causes Metabolic Syndrome by Impairing Dopamine Signaling in Striatal D1 Neurons
- NSUN4 Is a Dual Function Mitochondrial Protein Required for Both Methylation of 12S rRNA and Coordination of Mitoribosomal Assembly
- MicroRNA-133 Inhibits Behavioral Aggregation by Controlling Dopamine Synthesis in Locusts
- Convergence of Light and ABA Signaling on the Promoter
- Arf4 Is Required for Mammalian Development but Dispensable for Ciliary Assembly
- Distinct Requirements for Cranial Ectoderm and Mesenchyme-Derived Wnts in Specification and Differentiation of Osteoblast and Dermal Progenitors
- Chk2 and P53 Regulate the Transmission of Healed Chromosomes in the Male Germline
- Ddc2 Mediates Mec1 Activation through a Ddc1- or Dpb11-Independent Mechanism
- Mapping the Fitness Landscape of Gene Expression Uncovers the Cause of Antagonism and Sign Epistasis between Adaptive Mutations
- Euchromatic Transposon Insertions Trigger Production of Novel Pi- and Endo-siRNAs at the Target Sites in the Germline
- miR-100 Induces Epithelial-Mesenchymal Transition but Suppresses Tumorigenesis, Migration and Invasion
- Canine Hereditary Ataxia in Old English Sheepdogs and Gordon Setters Is Associated with a Defect in the Autophagy Gene Encoding
- Within-Host Spatiotemporal Dynamics of Plant Virus Infection at the Cellular Level
- Analysis of Meiosis in SUN1 Deficient Mice Reveals a Distinct Role of SUN2 in Mammalian Meiotic LINC Complex Formation and Function
- Genome-Wide Association Study of Metabolic Traits Reveals Novel Gene-Metabolite-Disease Links
- Mechanistically Distinct Mouse Models for -Associated Retinopathy
- DAF-16/FoxO Directly Regulates an Atypical AMP-Activated Protein Kinase Gamma Isoform to Mediate the Effects of Insulin/IGF-1 Signaling on Aging in
- Chromosome I Controls Chromosome II Replication in
- Integrated Genomic Characterization Reveals Novel, Therapeutically Relevant Drug Targets in FGFR and EGFR Pathways in Sporadic Intrahepatic Cholangiocarcinoma
- The Iodotyrosine Deiodinase Ortholog SUP-18 Functions through a Conserved Channel SC-Box to Regulate the Muscle Two-Pore Domain Potassium Channel SUP-9
- The Genome of Highlights a Fish Pathogen Adapted to Fluctuating Environments
- Distinct DNA Binding Sites Contribute to the TCF Transcriptional Switch in and
- The Streamlined Genome of spp. Relative to Human Pathogenic Kinetoplastids Reveals a Parasite Tailored for Plants
- PLOS Genetics
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Genome-Wide Association Study of Metabolic Traits Reveals Novel Gene-Metabolite-Disease Links
- A Cohesin-Independent Role for NIPBL at Promoters Provides Insights in CdLS
- Classic Selective Sweeps Revealed by Massive Sequencing in Cattle
- Arf4 Is Required for Mammalian Development but Dispensable for Ciliary Assembly
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy