-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
Three RNA Binding Proteins Form a Complex to Promote Differentiation of Germline Stem Cell Lineage in
In regenerative tissues, the successive differentiation of stem cell lineage is well controlled and coordinated with proper cell proliferation at each differentiation stage. Disruption of the control mechanism can lead to tumor growth or tissue degeneration. The germline stem cell lineage of Drosophila spermatogenesis provides an ideal research model to unravel the genetic network coordinating proliferation and differentiation. In a genetic screen, we identified a male-sterile mutant whose germ cells are under-differentiated and overproliferating. The responsible gene encodes an RNA-binding protein whose target belongs to a tumor suppressor family. We demonstrate that this and two other RNA-binding proteins form a physical and functional unit to ensure the proper differentiation and accurate proliferation of germline stem cell lineage.
Vyšlo v časopise: Three RNA Binding Proteins Form a Complex to Promote Differentiation of Germline Stem Cell Lineage in. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004797
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004797Souhrn
In regenerative tissues, the successive differentiation of stem cell lineage is well controlled and coordinated with proper cell proliferation at each differentiation stage. Disruption of the control mechanism can lead to tumor growth or tissue degeneration. The germline stem cell lineage of Drosophila spermatogenesis provides an ideal research model to unravel the genetic network coordinating proliferation and differentiation. In a genetic screen, we identified a male-sterile mutant whose germ cells are under-differentiated and overproliferating. The responsible gene encodes an RNA-binding protein whose target belongs to a tumor suppressor family. We demonstrate that this and two other RNA-binding proteins form a physical and functional unit to ensure the proper differentiation and accurate proliferation of germline stem cell lineage.
Zdroje
1. AlonsoL, FuchsE (2003) Stem cells in the skin: waste not, Wnt not. Genes & Development 17 : 1189–1200.
2. ClarkeMF, FullerM (2006) Stem cells and cancer: Two faces of eve. Cell 124 : 1111–1115.
3. KondoM, WagersAJ, ManzMG, ProhaskaSS, SchererDC, et al. (2003) Biology of hematopoietic stem cells and progenitors: Implications for clinical application. Annual Review of Immunology 21 : 759–806.
4. SchuijersJ, CleversH (2012) Adult mammalian stem cells: the role of Wnt, Lgr5 and R-spondins. Embo Journal 31 : 2685–2696.
5. JamiesonCHM, AillesLE, DyllaSJ, MuijtjensM, JonesC, et al. (2004) Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. New England Journal of Medicine 351 : 657–667.
6. KrivtsovAV, TwomeyD, FengZ, StubbsMC, WangY, et al. (2006) Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 442 : 818–822.
7. VisvaderJE (2011) Cells of origin in cancer. Nature 469 : 314–322.
8. de CuevasM, MatunisEL (2011) The stem cell niche: lessons from the Drosophila testis. Development 138 : 2861–2869.
9. FullerMT (1998) Genetic control of cell proliferation and differentiation in Drosophila spermatogenesis. Seminars in Cell & Developmental Biology 9 : 433–444.
10. SpradlingA, FullerMT, BraunRE, YoshidaS (2011) Germline stem cells. Cold Spring Harbor perspectives in biology 3: a002642–a002642.
11. ChangY-J, PiH, HsiehC-C, FullerMT (2013) Smurf-mediated differential proteolysis generates dynamic BMP signaling in germline stem cells during Drosophila testis development. Developmental Biology 383 : 106–120.
12. DaviesEL, LimJGY, JooWJ, TamCH, FullerMT (2013) The transcriptional regulator lola is required for stem cell maintenance and germ cell differentiation in the Drosophila testis. Developmental Biology 373 : 310–321.
13. EunSH, StoiberPM, WrightHJ, McMurdieKE, ChoiCH, et al. (2013) MicroRNAs downregulate Bag of marbles to ensure proper terminal differentiation in the Drosophila male germline. Development 140 : 23–30.
14. GonczyP, MatunisE, DiNardoS (1997) bag-of-marbles and benign gonial cell neoplasm act in the germline to restrict proliferation during Drosophila spermatogenesis. Development 124 : 4361–4371.
15. Insco MeganL, Bailey AlexisS, KimJ, Olivares GonzaloH, Wapinski OrlyL, et al. (2012) A self-limiting switch based on translational control regulates the transition from proliferation to differentiation in an adult stem cell lineage. Cell stem cell 11 : 689–700.
16. JotiP, Ghosh-RoyA, RayK (2011) Dynein light chain 1 functions in somatic cyst cells regulate spermatogonial divisions in Drosophila. Scientific Reports 1.
17. KigerAA, White-CooperH, FullerMT (2000) Somatic support cells restrict germline stem cell self-renewal and promote differentiation. Nature 407 : 750–754.
18. LiC-Y, GuoZ, WangZ (2007) TGF beta receptor saxophone non-autonomously regulates germline proliferation in a Smox/dSmad2-dependent manner in Drosophila testis. Developmental Biology 309 : 70–77.
19. MatunisE, TranJ, GonczyP, CaldwellK, DiNardoS (1997) punt and schnurri regulate a somatically derived signal that restricts proliferation of committed progenitors in the germline. Development 124 : 4383–4391.
20. ParrottBB, ChiangYT, HudsonA, SarkarA, GuichetA, et al. (2011) Nucleoporin98-96 Function Is Required for Transit Amplification Divisions in the Germ Line of Drosophila melanogaster. Plos One 6.
21. SarkarA, ParikhN, HearnSA, FullerMT, TazukeSI, et al. (2007) Antagonistic roles of Rac and Rho in organizing the germ cell microenvironment. Current Biology 17 : 1253–1258.
22. SchulzC, WoodCG, JonesDL, TazukeSI, FullerMT (2002) Signaling from germ cells mediated by the rhomboid homolog stet organizes encapsulation by somatic support cells. Development 129 : 4523–4534.
23. SunS, ZhaoS, WangZ (2008) Genes of Hippo signaling network act unconventionally in the control of germline proliferation in Drosophila. Developmental Dynamics 237 : 270–275.
24. TranJ, BrennerTJ, DiNardoS (2000) Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature 407 : 754–757.
25. ZhaoSW, ChenD, GengQ, WangZH (2013) The highly conserved LAMMER/CLK2 protein kinases prevent germ cell overproliferation in Drosophila. Developmental Biology 376 : 163–170.
26. InscoML, LeonA, TamCH, McKearinDM, FullerMT (2009) Accumulation of a differentiation regulator specifies transit amplifying division number in an adult stem cell lineage. Proceedings of the National Academy of Sciences of the United States of America 106 : 22311–22316.
27. McKearinDM, SpradlingAC (1990) bag-of-marbles - a Drosophila gene required to initiate both male and female gametogenesis. Genes & Development 4 : 2242–2251.
28. OhlsteinB, McKearinD (1997) Ectopic expression of the Drosophila Bam protein eliminates oogenic germline stem cells. Development 124 : 3651–3662.
29. ShengXR, BrawleyCM, MatunisEL (2009) Dedifferentiating Spermatogonia Outcompete Somatic Stem Cells for Niche Occupancy in the Drosophila Testis. Cell Stem Cell 5 : 191–203.
30. ShivdasaniAA, InghamPW (2003) Regulation of stem cell maintenance and transit amplifying cell proliferation by TGF-beta signaling in Drosophila spermatogenesis. Current Biology 13 : 2065–2072.
31. KimJY, LeeYC, KimC (2010) Direct inhibition of Pumilo activity by Bam and Bgcn in Drosophila germ line stem cell differentiation. Journal of Biological Chemistry 285 : 4741–4746.
32. LiY, MinorNT, ParkJK, McKearinDM, MainesJZ (2009) Bam and Bgcn antagonize Nanos-dependent germ-line stem cell maintenance. Proceedings of the National Academy of Sciences of the United States of America 106 : 9304–9309.
33. ShenR, WengC, YuJ, XieT (2009) eIF4A controls germline stem cell self-renewal by directly inhibiting BAM function in the Drosophila ovary. Proceedings of the National Academy of Sciences of the United States of America 106 : 11623–11628.
34. LiQ, LinS, WangX, LianG, LuZ, et al. (2009) Axin determines cell fate by controlling the p53 activation threshold after DNA damage. Nature Cell Biology 11 : 1128–U1184.
35. MorinX, DanemanR, ZavortinkM, ChiaW (2001) A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 98 : 15050–15055.
36. SarkarS, LakhotiaSC (2005) The Hsp60C gene in the 25F cytogenetic region in Drosophila melanogaster is essential for tracheal development and fertility. Journal of Genetics 84 : 265–281.
37. KawaseE, WongMD, DingBC, XieT (2004) Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 131 : 1365–1375.
38. PekJW, LimAK, KaiT (2009) Drosophila Maelstrom Ensures Proper Germline Stem Cell Lineage Differentiation by Repressing microRNA-7. Developmental Cell 17 : 417–424.
39. BernsteinDS, ButerN, StumpfC, WickensM (2002) Analyzing mRNA-protein complexes using a yeast three-hybrid system. Methods 26 : 123–141.
40. OhlsteinB, LavoieCA, VefO, GateffE, McKearinDM (2000) The Drosophila cystoblast differentiation factor, benign genial cell neoplasm, is related to DExH-box proteins and interacts genetically with bag-of-marbles. Genetics 155 : 1809–1819.
41. KyriakakisP, TippingM, AbedL, VeraksaA (2008) Tandem affinity purification in Drosophila - The advantages of the GS-TAP system. Fly 2 : 229–235.
42. XiaL, JiaS, HuangS, WangH, ZhuY, et al. (2010) The Fused/Smurf Complex Controls the Fate of Drosophila Germline Stem Cells by Generating a Gradient BMP Response. Cell 143 : 978–990.
43. MonkAC, SiddallNA, VolkT, FraserB, QuinnLM, et al. (2010) HOW is required for stem cell maintenance in the Drosophila testis and for the onset of transit-amplifying divisions. Cell Stem Cell 6 : 348–360.
44. SadaA, SuzukiA, SuzukiH, SagaY (2009) The RNA-Binding Protein NANOS2 Is Required to Maintain Murine Spermatogonial Stem Cells. Science 325 : 139–1398.
45. SaffmanEE, LaskoP (1999) Germline development in vertebrates and invertebrates. Cellular and Molecular Life Sciences 55 : 1141–1163.
46. ChauJ, KulnaneLS, SalzHK (2012) Sex-lethal enables germline stem cell differentiation by down-regulating Nanos protein levels during Drosophila oogenesis. Proceedings of the National Academy of Sciences of the United States of America 109 : 9465–9470.
47. LiY, ZhangQ, Carreira-RosarioA, MainesJZ, McKearinDM, et al. (2013) Mei-P26 Cooperates with Bam, Bgcn and Sxl to Promote Early Germline Development in the Drosophila Ovary. Plos One 8.
48. KeddeM, StrasserMJ, BoldajipourB, Oude VrielinkJA, SlanchevK, et al. (2007) RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131 : 1273–1286.
49. McKearinD, OhlsteinB (1995) A role for the Drosophila Bag-of-marbles protein in the differentiation of cystoblasts from germline stem-cells. Development 121 : 2937–2947.
50. ChenDH, McKearinD (2005) Gene circuitry controlling a stem cell niche. Current Biology 15 : 179–184.
51. ChenDH, McKearinDM (2003) A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 130 : 1159–1170.
52. JinZ, KirillyD, WengC, KawaseE, SongX, et al. (2008) Differentiation-defective stem cells outcompete normal stem cells for niche occupancy in the Drosophila ovary. Cell Stem Cell 2 : 39–49.
53. BuszczakM, PaternoS, LighthouseD, BachmanJ, PlanckJ, et al. (2007) The Carnegie protein trap library: A versatile tool for Drosophila developmental studies. Genetics 175 : 1505–1531.
54. EikenesAH, BrechA, StenmarkH, HaglundK (2013) Spatiotemporal control of Cindr at ring canals during incomplete cytokinesis in the Drosophila male germline. Developmental Biology 377 : 9–20.
55. SantelA, WinhauerT, BlumerN, RenkawitzPohlR (1997) The Drosophila don juan (dj) gene encodes a novel sperm specific protein component characterized by an unusual domain of a repetitive amino acid motif. Mechanisms of Development 64 : 19–30.
56. BrandAH, PerrimonN (1993) Targeted gene-expression as a means of altering cell fates and generating dominant phenotypes. Development 118 : 401–415.
57. Van DorenM, WilliamsonAL, LehmannR (1998) Regulation of zygotic gene expression in Drosophila primordial germ cells. Current Biology 8 : 243–246.
58. XuT, RubinGM (1993) Analysis of genetic mosaics in developing and adult drosophila tissues. Development 117 : 1223–1237.
59. HuangJ, ZhouW, DongW, WatsonAM, HongY (2009) Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering. Proceedings of the National Academy of Sciences of the United States of America 106 : 8284–8289.
60. BischofJ, MaedaRK, HedigerM, KarchF, BaslerK (2007) An optimized transgenesis system for Drosophila using germ-line-specific phi C31 integrases. Proceedings of the National Academy of Sciences of the United States of America 104 : 3312–3317.
61. RubinGM, SpradlingAC (1982) Genetic-transformation of drosophila with transposable element vectors. Science 218 : 348–353.
62. BuerckstuemmerT, BennettKL, PreradovicA, SchutzeG, HantschelO, et al. (2006) An efficient tandem affinity purification procedure for interaction proteomics in mammalian cells. Nature Methods 3 : 1013–1019.
63. VeraksaA, BauerA, Artavanis-TsakonasS (2005) Analyzing protein complexes in Drosophila with tandem affinity purification-mass spectrometry. Developmental Dynamics 232 : 827–834.
64. ChenD, WangQ, HuangH, XiaL, JiangX, et al. (2009) Effete-mediated degradation of Cyclin A is essential for the maintenance of germline stem cells in Drosophila. Development 136 : 4133–4142.
65. LiuJD, Valencia-SanchezMA, HannonGJ, ParkerR (2005) MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nature Cell Biology 7 : 719–U118.
66. PeritzT, ZengF, KannanayakalTJ, KilkK, EiriksdottirE, et al. (2006) Immunoprecipitation of mRNA-protein complexes. Nat Protoc 1 : 577–580.
Štítky
Genetika Reprodukčná medicína
Článek The COP9 Signalosome Converts Temporal Hormone Signaling to Spatial Restriction on Neural CompetenceČlánek Coordinate Regulation of Stem Cell Competition by Slit-Robo and JAK-STAT Signaling in the TestisČlánek The CSN/COP9 Signalosome Regulates Synaptonemal Complex Assembly during Meiotic Prophase I ofČlánek GPA: A Statistical Approach to Prioritizing GWAS Results by Integrating Pleiotropy and AnnotationČlánek Functional Diversity of Carbohydrate-Active Enzymes Enabling a Bacterium to Ferment Plant BiomassČlánek Heat-Induced Release of Epigenetic Silencing Reveals the Concealed Role of an Imprinted Plant GeneČlánek p53- and ERK7-Dependent Ribosome Surveillance Response Regulates Insulin-Like Peptide SecretionČlánek The Complex I Subunit Selectively Rescues Mutants through a Mechanism Independent of MitophagyČlánek Rad59-Facilitated Acquisition of Y′ Elements by Short Telomeres Delays the Onset of SenescenceČlánek ARTIST: High-Resolution Genome-Wide Assessment of Fitness Using Transposon-Insertion Sequencing
Článok vyšiel v časopisePLOS Genetics
Najčítanejšie tento týždeň
2014 Číslo 11- 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
- Establishing a Multidisciplinary Context for Modeling 3D Facial Shape from DNA
- RNA Processing Factors Swd2.2 and Sen1 Antagonize RNA Pol III-Dependent Transcription and the Localization of Condensin at Pol III Genes
- Inversion of the Chromosomal Region between Two Mating Type Loci Switches the Mating Type in
- A Thermolabile Aldolase A Mutant Causes Fever-Induced Recurrent Rhabdomyolysis without Hemolytic Anemia
- The Role of Regulatory Evolution in Maize Domestication
- Stress Granule-Defective Mutants Deregulate Stress Responsive Transcripts
- 24-Hour Rhythms of DNA Methylation and Their Relation with Rhythms of RNA Expression in the Human Dorsolateral Prefrontal Cortex
- Pseudoautosomal Region 1 Length Polymorphism in the Human Population
- Fungal Communication Requires the MAK-2 Pathway Elements STE-20 and RAS-2, the NRC-1 Adapter STE-50 and the MAP Kinase Scaffold HAM-5
- The COP9 Signalosome Converts Temporal Hormone Signaling to Spatial Restriction on Neural Competence
- The Protein -glucosyltransferase Rumi Modifies Eyes Shut to Promote Rhabdomere Separation in
- The Talin Head Domain Reinforces Integrin-Mediated Adhesion by Promoting Adhesion Complex Stability and Clustering
- Quantitative Genetics of CTCF Binding Reveal Local Sequence Effects and Different Modes of X-Chromosome Association
- Coordinate Regulation of Stem Cell Competition by Slit-Robo and JAK-STAT Signaling in the Testis
- Genetic Analysis of a Novel Tubulin Mutation That Redirects Synaptic Vesicle Targeting and Causes Neurite Degeneration in
- A Systems Genetics Approach Identifies , , and as Novel Aggressive Prostate Cancer Susceptibility Genes
- Three RNA Binding Proteins Form a Complex to Promote Differentiation of Germline Stem Cell Lineage in
- Approximation to the Distribution of Fitness Effects across Functional Categories in Human Segregating Polymorphisms
- The CSN/COP9 Signalosome Regulates Synaptonemal Complex Assembly during Meiotic Prophase I of
- SAS-1 Is a C2 Domain Protein Critical for Centriole Integrity in
- An RNA-Seq Screen of the Antenna Identifies a Transporter Necessary for Ammonia Detection
- GPA: A Statistical Approach to Prioritizing GWAS Results by Integrating Pleiotropy and Annotation
- Let's Face It—Complex Traits Are Just Not That Simple
- Glutamate Receptor Gene , Coffee, and Parkinson Disease
- The Red Queen Model of Recombination Hotspots Evolution in the Light of Archaic and Modern Human Genomes
- The Ethics of Our Inquiry: An Interview with Hank Greely
- Functional Diversity of Carbohydrate-Active Enzymes Enabling a Bacterium to Ferment Plant Biomass
- Regularized Machine Learning in the Genetic Prediction of Complex Traits
- Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response
- Lack of Replication of the -by-Coffee Interaction in Parkinson Disease
- Natural Polymorphisms in Human APOBEC3H and HIV-1 Vif Combine in Primary T Lymphocytes to Affect Viral G-to-A Mutation Levels and Infectivity
- A Germline Polymorphism of Thymine DNA Glycosylase Induces Genomic Instability and Cellular Transformation
- Heat-Induced Release of Epigenetic Silencing Reveals the Concealed Role of an Imprinted Plant Gene
- ATPase-Independent Type-III Protein Secretion in
- p53- and ERK7-Dependent Ribosome Surveillance Response Regulates Insulin-Like Peptide Secretion
- The Complex I Subunit Selectively Rescues Mutants through a Mechanism Independent of Mitophagy
- Evolution of DNA Methylation Patterns in the Brassicaceae is Driven by Differences in Genome Organization
- Regulation of mRNA Abundance by Polypyrimidine Tract-Binding Protein-Controlled Alternate 5′ Splice Site Choice
- Systematic Comparison of the Effects of Alpha-synuclein Mutations on Its Oligomerization and Aggregation
- Rad59-Facilitated Acquisition of Y′ Elements by Short Telomeres Delays the Onset of Senescence
- A Functional Portrait of Med7 and the Mediator Complex in
- Systematic Analysis of the Role of RNA-Binding Proteins in the Regulation of RNA Stability
- ARTIST: High-Resolution Genome-Wide Assessment of Fitness Using Transposon-Insertion Sequencing
- Genomic Evidence of Rapid and Stable Adaptive Oscillations over Seasonal Time Scales in Drosophila
- Genome-Wide Associations between Genetic and Epigenetic Variation Influence mRNA Expression and Insulin Secretion in Human Pancreatic Islets
- HAM-5 Functions As a MAP Kinase Scaffold during Cell Fusion in
- PLOS Genetics
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- An RNA-Seq Screen of the Antenna Identifies a Transporter Necessary for Ammonia Detection
- Systematic Comparison of the Effects of Alpha-synuclein Mutations on Its Oligomerization and Aggregation
- Functional Diversity of Carbohydrate-Active Enzymes Enabling a Bacterium to Ferment Plant Biomass
- Regularized Machine Learning in the Genetic Prediction of Complex Traits
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