Three RNA Binding Proteins Form a Complex to Promote Differentiation of Germline Stem Cell Lineage in

English version České info

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.1004797

Souhrn

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.