Poly(ADP-Ribose) Polymerase 1 (PARP-1) Regulates Ribosomal Biogenesis in Nucleoli

English version České info

Poly(ADP-ribose) polymerase 1 (PARP1), a nuclear protein, utilizes NAD to synthesize poly(AD-Pribose) (pADPr), resulting in both automodification and the modification of acceptor proteins. Substantial amounts of PARP1 and pADPr (up to 50%) are localized to the nucleolus, a subnuclear organelle known as a region for ribosome biogenesis and maturation. At present, the functional significance of PARP1 protein inside the nucleolus remains unclear. Using PARP1 mutants, we investigated the function of PARP1, pADPr, and PARP1-interacting proteins in the maintenance of nucleolus structure and functions. Our analysis shows that disruption of PARP1 enzymatic activity caused nucleolar disintegration and aberrant localization of nucleolar-specific proteins. Additionally, PARP1 mutants have increased accumulation of rRNA intermediates and a decrease in ribosome levels. Together, our data suggests that PARP1 enzymatic activity is required for targeting nucleolar proteins to the proximity of precursor rRNA; hence, PARP1 controls precursor rRNA processing, post-transcriptional modification, and pre-ribosome assembly. Based on these findings, we propose a model that explains how PARP1 activity impacts nucleolar functions and, consequently, ribosomal biogenesis.

Vyšlo v časopise: Poly(ADP-Ribose) Polymerase 1 (PARP-1) Regulates Ribosomal Biogenesis in Nucleoli. PLoS Genet 8(1): e32767. doi:10.1371/journal.pgen.1002442
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002442

Souhrn

Zdroje

1. BoisvertFMvan KoningsbruggenSNavascuesJLamondAI 2007 The multifunctional nucleolus. Nat Rev Mol Cell Biol 8 574 585

2. FrankDJEdgarBARothMB 2002 The Drosophila melanogaster gene brain tumor negatively regulates cell growth and ribosomal RNA synthesis. Development 129 399 407

3. RogerBMoisandAAmalricFBouvetP 2002 Repression of RNA polymerase I transcription by nucleolin is independent of the RNA sequence that is transcribed. J Biol Chem 277 10209 10219

4. TautzDHancockJMWebbDATautzCDoverGA 1988 Complete sequences of the rRNA genes of Drosophila melanogaster. Mol Biol Evol 5 366 376

5. PrietoJLMcStayB 2005 Nucleolar biogenesis: the first small steps. Biochem Soc Trans 33 1441 1443

6. MilkereitPGadalOPodtelejnikovATrumtelSGasN 2001 Maturation and intranuclear transport of pre-ribosomes requires Noc proteins. Cell 105 499 509

7. BelinSBeghinASolano-GonzalezEBezinLBrunet-ManquatS 2009 Dysregulation of ribosome biogenesis and translational capacity is associated with tumor progression of human breast cancer cells. PLoS ONE 4 e7147 doi:10.1371/journal.pone.0007147

8. D'AmoursDDesnoyersSD'SilvaIPoirierGG 1999 Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342 Pt 2 249 268

9. AubinRJFrechetteAde MurciaGMandelPLordA 1983 Correlation between endogenous nucleosomal hyper(ADP-ribosyl)ation of histone H1 and the induction of chromatin relaxation. EMBO J 2 1685 1693

10. BoulikasT 1990 Poly(ADP-ribosylated) histones in chromatin replication. J Biol Chem 265 14638 14647

11. JiYTulinAV 2010 The roles of PARP1 in gene control and cell differentiation. Curr Opin Genet Dev 20 512 518

12. KrupitzaGCeruttiP 1989 Poly(ADP-ribosylation) of histones in intact human keratinocytes. Biochemistry 28 4054 4060

13. SchreiberVDantzerFAmeJCde MurciaG 2006 Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7 517 528

14. Mendoza-AlvarezHAlvarez-GonzalezR 2001 Regulation of p53 sequence-specific DNA-binding by covalent poly(ADP-ribosyl)ation. J Biol Chem 276 36425 36430

15. MalangaMPleschkeJMKleczkowskaHEAlthausFR 1998 Poly(ADP-ribose) binds to specific domains of p53 and alters its DNA binding functions. J Biol Chem 273 11839 11843

16. PleschkeJMKleczkowskaHEStrohmMAlthausFR 2000 Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J Biol Chem 275 40974 40980

17. RealeAMatteisGDGalleazziGZampieriMCaiafaP 2005 Modulation of DNMT1 activity by ADP-ribose polymers. Oncogene 24 13 19

18. DavidovicLVodenicharovMAffarEBPoirierGG 2001 Importance of poly(ADP-ribose) glycohydrolase in the control of poly(ADP-ribose) metabolism. Exp Cell Res 268 7 13

19. HanaiSKanaiMOhashiSOkamotoKYamadaM 2004 Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster. Proc Natl Acad Sci U S A 101 82 86

20. KotovaEJarnikMTulinAV 2009 Poly (ADP-ribose) polymerase 1 is required for protein localization to Cajal body. PLoS Genet 5 e1000387 doi:10.1371/journal.pgen.1000387

21. TulinANaumovaNMMenonAKSpradlingAC 2006 Drosophila poly(ADP-ribose) glycohydrolase mediates chromatin structure and SIR2-dependent silencing. Genetics 172 363 371

22. Mendoza-AlvarezHAlvarez-GonzalezR 1993 Poly(ADP-ribose) polymerase is a catalytic dimer and the automodification reaction is intermolecular. J Biol Chem 268 22575 22580

23. TulinAStewartDSpradlingAC 2002 The Drosophila heterochromatic gene encoding poly(ADP-ribose) polymerase (PARP) is required to modulate chromatin structure during development. Genes Dev 16 2108 2119

24. TulinASpradlingA 2003 Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci. Science 299 560 562

25. DesnoyersSKaufmannSHPoirierGG 1996 Alteration of the nucleolar localization of poly(ADP-ribose) polymerase upon treatment with transcription inhibitors. Exp Cell Res 227 146 153

26. MederVSBoeglinMde MurciaGSchreiberV 2005 PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli. J Cell Sci 118 211 222

27. ChanPK 1992 Characterization and cellular localization of nucleophosmin/B23 in HeLa cells treated with selected cytotoxic agents (studies of B23-translocation mechanism). Exp Cell Res 203 174 181

28. LeitingerNWesierska-GadekJ 1993 ADP-ribosylation of nucleolar proteins in HeLa tumor cells. J Cell Biochem 52 153 158

29. KoyamaYKatagiriSHanaiSUchidaKMiwaM 1999 Poly(ADP-ribose) polymerase interacts with novel Drosophila ribosomal proteins, L22 and l23a, with unique histone-like amino-terminal extensions. Gene 226 339 345

30. PinnolaANaumovaNShahMTulinAV 2007 Nucleosomal core histones mediate dynamic regulation of poly(ADP-ribose) polymerase 1 protein binding to chromatin and induction of its enzymatic activity. J Biol Chem 282 32511 32519

31. TollerveyDLehtonenHCarmo-FonsecaMHurtEC 1991 The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J 10 573 583

32. KotovaEJarnikMTulinAV 2010 Uncoupling of the transactivation and transrepression functions of PARP1 protein. Proc Natl Acad Sci U S A 107 6406 6411

33. BuszczakMPaternoSLighthouseDBachmanJPlanckJ 2007 The carnegie protein trap library: a versatile tool for Drosophila developmental studies. Genetics 175 1505 1531

34. VorbruggenGOnelSJackleH 2000 Restricted expression and subnuclear localization of the Drosophila gene Dnop5, a member of the Nop/Sik family of the conserved rRNA processing factors. Mech Dev 90 305 308

35. GinistyHSicardHRogerBBouvetP 1999 Structure and functions of nucleolin. J Cell Sci 112 Pt 6 761 772

36. BierhoffHDundrMMichelsAAGrummtI 2008 Phosphorylation by casein kinase 2 facilitates rRNA gene transcription by promoting dissociation of TIF-IA from elongating RNA polymerase I. Mol Cell Biol 28 4988 4998

37. BergesTPetfalskiETollerveyDHurtEC 1994 Synthetic lethality with fibrillarin identifies NOP77p, a nucleolar protein required for pre-rRNA processing and modification. EMBO J 13 3136 3148

38. JansenRTollerveyDHurtEC 1993 A U3 snoRNP protein with homology to splicing factor PRP4 and G beta domains is required for ribosomal RNA processing. EMBO J 12 2549 2558

39. SchimmangTTollerveyDKernHFrankRHurtEC 1989 A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability. EMBO J 8 4015 4024

40. PerryRP 1976 Processing of RNA. Annu Rev Biochem 45 605 629

41. WinicovIPerryRP 1975 Enzymological aspects of processing of mammalian rRNA. Brookhaven Symp Biol 201 213

42. Bailey-SerresJ 1999 Selective translation of cytoplasmic mRNAs in plants. Trends Plant Sci 4 142 148

43. MontanaroLTrereDDerenziniM 2008 Nucleolus, ribosomes, and cancer. Am J Pathol 173 301 310

44. OlsonMOHingoraniKSzebeniA 2002 Conventional and nonconventional roles of the nucleolus. Int Rev Cytol 219 199 266

45. RubbiCPMilnerJ 2003 Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 22 6068 6077

46. GuerreroPAMaggertKA 2011 The CCCTC-binding factor (CTCF) of Drosophila contributes to the regulation of the ribosomal DNA and nucleolar stability. PLoS ONE 6 e16401 doi:10.1371/journal.pone.0016401

47. MandalRKDawidIB 1981 The nucleotide sequence at the transcription termination site of ribosomal RNA in Drosophila melanogaster. Nucleic Acids Res 9 1801 1811

48. PeteschSJLisJT 2008 Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci. Cell 134 74 84

49. TulinAChinenovYSpradlingA 2003 Regulation of chromatin structure and gene activity by poly(ADP-ribose) polymerases. Curr Top Dev Biol 56 55 83

50. KobayashiT 2011 Regulation of ribosomal RNA gene copy number and its role in modulating genome integrity and evolutionary adaptability in yeast. Cell Mol Life Sci 68 1395 1403

51. SkidmoreCJDaviesMIGoodwinPMHalldorssonHLewisPJ 1979 The involvement of poly(ADP-ribose) polymerase in the degradation of NAD caused by gamma-radiation and N-methyl-N-nitrosourea. Eur J Biochem 101 135 142

52. DurkaczBWOmidijiOGrayDAShallS 1980 (ADP-ribose)n participates in DNA excision repair. Nature 283 593 596

53. 1999 The FlyBase database of the Drosophila Genome Projects and community literature. The FlyBase Consortium. Nucleic Acids Res 27 85 88

54. Artavanis-TsakonasS 2004 Accessing the Exelixis collection. Nat Genet 36 207

55. ManseauLBaradaranABrowerDBudhuAElefantF 1997 GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev Dyn 209 310 322

56. CassoDRamirez-WeberFKornbergTB 2000 GFP-tagged balancer chromosomes for Drosophila melanogaster. Mech Dev 91 451 454

57. SpradlingACRubinGM 1982 Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218 341 347

58. ProkhorovaAVVoloshinaMAShostakNGBarskiiVEGolubovskiiMD 1994 [Preparation and primary genetic analysis of Drosophila melanogaster transformants line w'lz(b)/XXywf, containing mini-white genes, integrated in the genome during P-element-dependent transformation]. Genetika 30 874 878

59. DernburgAFSedatJWHawleyRS 1996 Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86 135 146