The TRIM-NHL Protein LIN-41 Controls the Onset of Developmental Plasticity in

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Reprogramming into a naïve, pluripotent state during the oocyte-to-embryo transition is directed by the oocyte cytoplasm. To understand how this reprogramming is controlled, we searched for C. elegans mutants in which the activation of embryonic genome, a landmark event demarcating the switch from a germline -⁠ to embryo-specific transcription, is initiated precociously in germ cells. This screen identified a novel function for LIN-41, a member of the TRIM-NHL protein family, in preventing a premature onset of embryonic-like differentiation and teratoma formation in developing oocytes, thus ensuring a successful passage between generations. This is the first example of such a regulator in cells that are poised for embryonic development. Interestingly, the majority of molecular “roadblocks” to reprograming that have been identified so far are epigenetic regulators. However, we propose that, at least in germ cells, LIN-41-like regulators may fulfill an analogous role in the cytoplasm, which has possible implications for the generation of human pluripotent stem cells.

Vyšlo v časopise: The TRIM-NHL Protein LIN-41 Controls the Onset of Developmental Plasticity in. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004533
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004533

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Zdroje

1. GurdonJB, MeltonDA (2008) Nuclear reprogramming in cells. Science 322 : 1811–1815.

2. YuJ, ThomsonJA (2008) Pluripotent stem cell lines. Genes Dev 22 : 1987–1997.

3. PatelT, TursunB, RaheDP, HobertO (2012) Removal of Polycomb repressive complex 2 makes C. elegans germ cells susceptible to direct conversion into specific somatic cell types. Cell Rep 2 : 1178–1186.

4. TursunB, PatelT, KratsiosP, HobertO (2011) Direct conversion of C. elegans germ cells into specific neuron types. Science 331 : 304–308.

5. Kaser-PebernardS, MullerF, WickyC (2014) LET-418/Mi2 and SPR-5/LSD1 Cooperatively Prevent Somatic Reprogramming of C. elegans Germline Stem Cells. Stem Cell Reports 2 : 547–559.

6. CioskR, DePalmaM, PriessJR (2006) Translational regulators maintain totipotency in the Caenorhabditis elegans germline. Science 311 : 851–853.

7. WrightJE, CioskR (2013) RNA-based regulation of pluripotency. Trends Genet 29 : 99–107.

8. AkkersRC, van HeeringenSJ, JacobiUG, Janssen-MegensEM, FrancoijsKJ, et al. (2009) A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos. Dev Cell 17 : 425–434.

9. VastenhouwNL, ZhangY, WoodsIG, ImamF, RegevA, et al. (2010) Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464 : 922–926.

10. WulczynFG, CuevasE, FranzoniE, RybakA (2011) miRNAs Need a Trim : Regulation of miRNA Activity by Trim-NHL Proteins. Adv Exp Med Biol 700 : 85–105.

11. RybakA, FuchsH, HadianK, SmirnovaL, WulczynEA, et al. (2009) The let-7 target gene mouse lin-41 is a stem cell specific E3 ubiquitin ligase for the miRNA pathway protein Ago2. Nat Cell Biol 11 : 1411–1420.

12. KudryashovaE, KudryashovD, KramerovaI, SpencerMJ (2005) Trim32 is a ubiquitin ligase mutated in limb girdle muscular dystrophy type 2H that binds to skeletal muscle myosin and ubiquitinates actin. J Mol Biol 354 : 413–424.

13. RahejaR, LiuY, HukkelhovenE, YehN, KoffA (2014) The ability of TRIM3 to induce growth arrest depends on RING-dependent E3 ligase activity. Biochem J 458 : 537–545.

14. KwonSC, YiH, EichelbaumK, FohrS, FischerB, et al. (2013) The RNA-binding protein repertoire of embryonic stem cells. Nat Struct Mol Biol 20 : 1122–1130.

15. LoedigeI, StotzM, QamarS, KramerK, HennigJ, et al. (2014) The NHL domain of BRAT is an RNA-binding domain that directly contacts the hunchback mRNA for regulation. Genes Dev 28 : 749–764.

16. LoerB, BauerR, BornheimR, GrellJ, KremmerE, et al. (2008) The NHL-domain protein Wech is crucial for the integrin-cytoskeleton link. Nat Cell Biol 10 : 422–428.

17. LiuY, RahejaR, YehN, CiznadijaD, PedrazaAM, et al. (2014) TRIM3, a tumor suppressor linked to regulation of p21(Waf1/Cip1.). Oncogene 33 : 308–315.

18. ChangHM, MartinezNJ, ThorntonJE, HaganJP, NguyenKD, et al. (2012) Trim71 cooperates with microRNAs to repress Cdkn1a expression and promote embryonic stem cell proliferation. Nat Commun 3 : 923.

19. LoedigeI, GaidatzisD, SackR, MeisterG, FilipowiczW (2013) The mammalian TRIM-NHL protein TRIM71/LIN-41 is a repressor of mRNA function. Nucleic Acids Res 41 : 518–532.

20. LeeSH, ChoS, Sun KimM, ChoiK, ChoJY, et al. (2014) The ubiquitin ligase human TRIM71 regulates let-7 microRNA biogenesis via modulation of Lin28B protein. Biochim Biophys Acta 1839 : 374–386.

21. AramaE, DickmanD, KimchieZ, ShearnA, LevZ (2000) Mutations in the beta-propeller domain of the Drosophila brain tumor (brat) protein induce neoplasm in the larval brain. Oncogene 19 : 3706–3716.

22. FrankDJ, EdgarBA, RothMB (2002) The Drosophila melanogaster gene brain tumor negatively regulates cell growth and ribosomal RNA synthesis. Development 129 : 399–407.

23. BetschingerJ, MechtlerK, KnoblichJA (2006) Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell 124 : 1241–1253.

24. LeeCY, WilkinsonBD, SiegristSE, WhartonRP, DoeCQ (2006) Brat is a Miranda cargo protein that promotes neuronal differentiation and inhibits neuroblast self-renewal. Dev Cell 10 : 441–449.

25. NeumullerRA, BetschingerJ, FischerA, BushatiN, PoernbacherI, et al. (2008) Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature 454 : 241–245.

26. FroskP, WeilerT, NylenE, SudhaT, GreenbergCR, et al. (2002) Limb-girdle muscular dystrophy type 2H associated with mutation in TRIM32, a putative E3-ubiquitin-ligase gene. Am J Hum Genet 70 : 663–672.

27. ChiangAP, BeckJS, YenHJ, TayehMK, ScheetzTE, et al. (2006) Homozygosity mapping with SNP arrays identifies TRIM32, an E3 ubiquitin ligase, as a Bardet-Biedl syndrome gene (BBS11). Proc Natl Acad Sci U S A 103 : 6287–6292.

28. WorringerKA, RandTA, HayashiY, SamiS, TakahashiK, et al. (2014) The let-7/LIN-41 pathway regulates reprogramming to human induced pluripotent stem cells by controlling expression of prodifferentiation genes. Cell Stem Cell 14 : 40–52.

29. SlackFJ, BassonM, LiuZ, AmbrosV, HorvitzHR, et al. (2000) The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor. Mol Cell 5 : 659–669.

30. EcsediM, GrosshansH (2013) LIN-41/TRIM71: emancipation of a miRNA target. Genes Dev 27 : 581–589.

31. BiedermannB, WrightJ, SenftenM, KalchhauserI, SarathyG, et al. (2009) Translational repression of cyclin E prevents precocious mitosis and embryonic gene activation during C. elegans meiosis. Dev Cell 17 : 355–364.

32. SeydouxG, MelloCC, PettittJ, WoodWB, PriessJR, et al. (1996) Repression of gene expression in the embryonic germ lineage of C. elegans. Nature 382 : 713–716.

33. SeydouxG, DunnMA (1997) Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster. Development 124 : 2191–2201.

34. StitzelML, SeydouxG (2007) Regulation of the oocyte-to-zygote transition. Science 316 : 407–408.

35. GrantB, HirshD (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10 : 4311–4326.

36. KawasakiI, ShimYH, KirchnerJ, KaminkerJ, WoodWB, et al. (1998) PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 94 : 635–645.

37. McGinnisW, KrumlaufR (1992) Homeobox genes and axial patterning. Cell 68 : 283–302.

38. HunterCP, KenyonC (1996) Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos. Cell 87 : 217–226.

39. LeiH, LiuJ, FukushigeT, FireA, KrauseM (2009) Caudal-like PAL-1 directly activates the bodywall muscle module regulator hlh-1 in C. elegans to initiate the embryonic muscle gene regulatory network. Development 136 : 1241–1249.

40. MootzD, HoDM, HunterCP (2004) The STAR/Maxi-KH domain protein GLD-1 mediates a developmental switch in the translational control of C. elegans PAL-1. Development 131 : 3263–3272.

41. HsuJY, SunZW, LiX, ReubenM, TatchellK, et al. (2000) Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102 : 279–291.

42. ZetkaMC, KawasakiI, StromeS, MullerF (1999) Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev 13 : 2258–2270.

43. AlbertsonDG, ThomsonJN (1993) Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res 1 : 15–26.

44. Mikeladze-DvaliT, von TobelL, StrnadP, KnottG, LeonhardtH, et al. (2012) Analysis of centriole elimination during C. elegans oogenesis. Development 139 : 1670–1679.

45. KempCA, KopishKR, ZipperlenP, AhringerJ, O'ConnellKF (2004) Centrosome maturation and duplication in C. elegans require the coiled-coil protein SPD-2. Dev Cell 6 : 511–523.

46. StringhamEG, DixonDK, JonesD, CandidoEP (1992) Temporal and spatial expression patterns of the small heat shock (hsp16) genes in transgenic Caenorhabditis elegans. Mol Biol Cell 3 : 221–233.

47. ReinkeV, GilIS, WardS, KazmerK (2004) Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131 : 311–323.

48. BudhidarmoR, NakataniY, DayCL (2012) RINGs hold the key to ubiquitin transfer. Trends Biochem Sci 37 : 58–65.

49. BorkP, HolmL, SanderC (1994) The immunoglobulin fold. Structural classification, sequence patterns and common core. J Mol Biol 242 : 309–320.

50. HolmL, RosenstromP (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38: W545–549.

51. KrissinelE, HenrickK (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372 : 774–797.

52. EdwardsTA, WilkinsonBD, WhartonRP, AggarwalAK (2003) Model of the brain tumor-Pumilio translation repressor complex. Genes Dev 17 : 2508–2513.

53. PageMF, CarrB, AndersKR, GrimsonA, AndersonP (1999) SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol Cell Biol 19 : 5943–5951.

54. HarrisRE, PargettM, SutcliffeC, UmulisD, AsheHL (2011) Brat promotes stem cell differentiation via control of a bistable switch that restricts BMP signaling. Dev Cell 20 : 72–83.

55. UpdikeDL, KnutsonAK, EgelhoferTA, CampbellAC, StromeS (2014) Germ-Granule Components Prevent Somatic Development in the C. elegans Germline. Curr Biol 24 : 970–975.

56. BrodiganTM, LiuJ, ParkM, KipreosET, KrauseM (2003) Cyclin E expression during development in Caenorhabditis elegans. Dev Biol 254 : 102–115.

57. ReinhartBJ, SlackFJ, BassonM, PasquinelliAE, BettingerJC, et al. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403 : 901–906.

58. VellaMC, ChoiEY, LinSY, ReinertK, SlackFJ (2004) The C. elegans microRNA let-7 binds to imperfect let-7 complementary sites from the lin-41 3′UTR. Genes Dev 18 : 132–137.

59. SchwambornJC, BerezikovE, KnoblichJA (2009) The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136 : 913–925.

60. ZouY, ChiuH, ZinovyevaA, AmbrosV, ChuangCF, et al. (2013) Developmental decline in neuronal regeneration by the progressive change of two intrinsic timers. Science 340 : 372–376.

61. Maller SchulmanBR, LiangX, StahlhutC, DelConteC, StefaniG, et al. (2008) The let-7 microRNA target gene, Mlin41/Trim71 is required for mouse embryonic survival and neural tube closure. Cell Cycle 7 : 3935–3942.

62. SchulmanBR, Esquela-KerscherA, SlackFJ (2005) Reciprocal expression of lin-41 and the microRNAs let-7 and mir-125 during mouse embryogenesis. Dev Dyn 234 : 1046–1054.

63. KnoepflerPS (2008) Why myc? An unexpected ingredient in the stem cell cocktail. Cell Stem Cell 2 : 18–21.

64. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77 : 71–94.

65. ZurynS, Le GrasS, JametK, JarriaultS (2010) A strategy for direct mapping and identification of mutations by whole-genome sequencing. Genetics 186 : 427–430.

66. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 : 1754–1760.

67. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 : 2078–2079.

68. DePristoMA, BanksE, PoplinR, GarimellaKV, MaguireJR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43 : 491–498.

69. DrakeJW, BaltzRH (1976) The biochemistry of mutagenesis. Annu Rev Biochem 45 : 11–37.

70. LinR, HillRJ, PriessJR (1998) POP-1 and anterior-posterior fate decisions in C. elegans embryos. Cell 92 : 229–239.

71. PriessJR, ThomsonJN (1987) Cellular interactions in early C. elegans embryos. Cell 48 : 241–250.

72. ScheckelC, GaidatzisD, WrightJE, CioskR (2012) Genome-wide analysis of GLD-1-mediated mRNA regulation suggests a role in mRNA storage. PLoS Genet 8: e1002742.

73. NavarroRE, ShimEY, KoharaY, SingsonA, BlackwellTK (2001) cgh-1, a conserved predicted RNA helicase required for gametogenesis and protection from physiological germline apoptosis in C. elegans. Development 128 : 3221–3232.

74. ChapmanRD, HeidemannM, AlbertTK, MailhammerR, FlatleyA, et al. (2007) Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 318 : 1780–1782.

75. BurgerJ, MerletJ, TavernierN, RichaudeauB, ArnoldA, et al. (2013) CRL2(LRR-1) E3-ligase regulates proliferation and progression through meiosis in the Caenorhabditis elegans germline. PLoS Genet 9: e1003375.

76. BerrowNS, AldertonD, OwensRJ (2009) The precise engineering of expression vectors using high-throughput In-Fusion PCR cloning. Methods Mol Biol 498 : 75–90.

77. KabschW (2010) Xds. Acta Crystallogr D Biol Crystallogr 66 : 125–132.

78. McCoyAJ, Grosse-KunstleveRW, AdamsPD, WinnMD, StoroniLC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40 : 658–674.

79. CowtanK (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62 : 1002–1011.

80. AfoninePV, Grosse-KunstleveRW, EcholsN, HeaddJJ, MoriartyNW, et al. (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr D Biol Crystallogr 68 : 352–367.

81. EmsleyP, LohkampB, ScottWG, CowtanK (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66 : 486–501.

82. Bricogne G., Blanc E., Brandl M., Flensburg C., Keller P et al. (2011). BUSTER Version 2.11.4, Cambridge, United Kingdom: Global Phasing Ltd.

83. SodingJ, BiegertA, LupasAN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33: W244–248.