#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

The SMC Loader Scc2 Promotes ncRNA Biogenesis and Translational Fidelity


The structure of chromosomes contributes to the production of RNAs. Chromosome structure is maintained in part by an evolutionarily conserved group of proteins known as structural maintenance of chromosomes proteins. These proteins are loaded onto chromosomes by a second evolutionarily conserved protein complex known as Scc2-Scc4. The Scc2 component is often mutated in a human developmental disorder known as Cornelia de Lange syndrome. We find that Scc2 in budding yeast is important for the production of a group of RNAs known as snoRNAs. These RNAs play a critical role in ribosome production; without them the fidelity of ribosomes suffers. Ribosomes are the molecular machines that translate mRNAs to proteins. Scc2 is also important for the production of the RNA components of ribosomes. Our findings suggest Scc2 normally promotes the production of RNAs that support translational fidelity. We hypothesize that defects in protein synthesis may contribute to Cornelia de Lange syndrome.


Vyšlo v časopise: The SMC Loader Scc2 Promotes ncRNA Biogenesis and Translational Fidelity. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005308
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005308

Souhrn

The structure of chromosomes contributes to the production of RNAs. Chromosome structure is maintained in part by an evolutionarily conserved group of proteins known as structural maintenance of chromosomes proteins. These proteins are loaded onto chromosomes by a second evolutionarily conserved protein complex known as Scc2-Scc4. The Scc2 component is often mutated in a human developmental disorder known as Cornelia de Lange syndrome. We find that Scc2 in budding yeast is important for the production of a group of RNAs known as snoRNAs. These RNAs play a critical role in ribosome production; without them the fidelity of ribosomes suffers. Ribosomes are the molecular machines that translate mRNAs to proteins. Scc2 is also important for the production of the RNA components of ribosomes. Our findings suggest Scc2 normally promotes the production of RNAs that support translational fidelity. We hypothesize that defects in protein synthesis may contribute to Cornelia de Lange syndrome.


Zdroje

1. Michaelis C, Ciosk R, Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell. 1997 Oct 3;91(1):35–45. 9335333

2. Gruber S, Haering CH, Nasmyth K. Chromosomal cohesin forms a ring. Cell. 2003 Mar 21;112(6):765–77. 12654244

3. Haering CH, Lowe J, Hochwagen A, Nasmyth K. Molecular architecture of SMC proteins and the yeast cohesin complex. Molecular cell. 2002 Apr;9(4):773–88. 11983169

4. Strunnikov AV, Larionov VL, Koshland D. SMC1: an essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous protein family. The Journal of cell biology. 1993 Dec;123(6 Pt 2):1635–48. 8276886

5. D'Ambrosio C, Schmidt CK, Katou Y, Kelly G, Itoh T, Shirahige K, et al. Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes & development. 2008 Aug 15;22(16):2215–27.

6. Dowen JM, Bilodeau S, Orlando DA, Hubner MR, Abraham BJ, Spector DL, et al. Multiple structural maintenance of chromosome complexes at transcriptional regulatory elements. Stem cell reports. 2013;1(5):371–8. doi: 10.1016/j.stemcr.2013.09.002 24286025

7. Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Shevchenko A, et al. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Molecular cell. 2000 Feb;5(2):243–54. 10882066

8. Unal E, Arbel-Eden A, Sattler U, Shroff R, Lichten M, Haber JE, et al. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Molecular cell. 2004 Dec 22;16(6):991–1002. 15610741

9. Rollins RA, Korom M, Aulner N, Martens A, Dorsett D. Drosophila nipped-B protein supports sister chromatid cohesion and opposes the stromalin/Scc3 cohesion factor to facilitate long-range activation of the cut gene. Molecular and cellular biology. 2004 Apr;24(8):3100–11. 15060134

10. Horsfield JA, Anagnostou SH, Hu JK, Cho KH, Geisler R, Lieschke G, et al. Cohesin-dependent regulation of Runx genes. Development. 2007 Jul;134(14):2639–49. 17567667

11. Misulovin Z, Schwartz YB, Li XY, Kahn TG, Gause M, MacArthur S, et al. Association of cohesin and Nipped-B with transcriptionally active regions of the Drosophila melanogaster genome. Chromosoma. 2008 Feb;117(1):89–102. 17965872

12. Lopez-Serra L, Kelly G, Patel H, Stewart A, Uhlmann F. The Scc2-Scc4 complex acts in sister chromatid cohesion and transcriptional regulation by maintaining nucleosome-free regions. Nature genetics. 2014 Oct;46(10):1147–51. doi: 10.1038/ng.3080 25173104

13. Mannini L, Cucco F, Quarantotti V, Krantz ID, Musio A. Mutation spectrum and genotype-phenotype correlation in Cornelia de Lange syndrome. Human mutation. 2013 Dec;34(12):1589–96. doi: 10.1002/humu.22430 24038889

14. Liu J, Zhang Z, Bando M, Itoh T, Deardorff MA, Clark D, et al. Transcriptional dysregulation in NIPBL and cohesin mutant human cells. PLoS biology. 2009 May 5;7(5):e1000119. doi: 10.1371/journal.pbio.1000119 19468298

15. Kaur M, DeScipio C, McCallum J, Yaeger D, Devoto M, Jackson LG, et al. Precocious sister chromatid separation (PSCS) in Cornelia de Lange syndrome. American journal of medical genetics Part A. 2005 Sep 15;138(1):27–31. 16100726

16. Xu B, Sowa N, Cardenas ME, Gerton JL. l-leucine partially rescues translational and developmental defects associated with zebrafish models of Cornelia de Lange syndrome. Human molecular genetics. 2014 Nov 6.

17. Lindgren E, Hagg S, Giordano F, Bjorkegren J, Strom L. Inactivation of the Budding Yeast Cohesin Loader Scc2 alters Gene Expression both Globally and in Response to a Single DNA Double Strand Break. Cell cycle. 2014 Sep 19:0.

18. Schwartz S, Bernstein DA, Mumbach MR, Jovanovic M, Herbst RH, Leon-Ricardo BX, et al. Transcriptome-wide Mapping Reveals Widespread Dynamic-Regulated Pseudouridylation of ncRNA and mRNA. Cell. 2014 Sep 25;159(1):148–62. doi: 10.1016/j.cell.2014.08.028 25219674

19. Carlile TM, Rojas-Duran MF, Zinshteyn B, Shin H, Bartoli KM, Gilbert WV. Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature. 2014 Sep 5.

20. Ofengand J. Ribosomal RNA pseudouridines and pseudouridine synthases. FEBS letters. 2002 Mar 6;514(1):17–25. 11904174

21. Hu B, Itoh T, Mishra A, Katoh Y, Chan KL, Upcher W, et al. ATP hydrolysis is required for relocating cohesin from sites occupied by its Scc2/4 loading complex. Current biology: CB. 2011 Jan 11;21(1):12–24. doi: 10.1016/j.cub.2010.12.004 21185190

22. Bose T, Lee KK, Lu S, Xu B, Harris B, Slaughter B, et al. Cohesin proteins promote ribosomal RNA production and protein translation in yeast and human cells. PLoS genetics. 2012;8(6):e1002749. doi: 10.1371/journal.pgen.1002749 22719263

23. Harris B, Bose T, Lee KK, Wang F, Lu S, Ross RT, et al. Cohesion promotes nucleolar structure and function. Molecular biology of the cell. 2014 Feb;25(3):337–46. doi: 10.1091/mbc.E13-07-0377 24307683

24. Zhang Y, Sikes ML, Beyer AL, Schneider DA. The Paf1 complex is required for efficient transcription elongation by RNA polymerase I. Proceedings of the National Academy of Sciences of the United States of America. 2009 Feb 17;106(7):2153–8. doi: 10.1073/pnas.0812939106 19164765

25. Reichow SL, Hamma T, Ferre-D'Amare AR, Varani G. The structure and function of small nucleolar ribonucleoproteins. Nucleic acids research. 2007;35(5):1452–64. 17284456

26. Jack K, Bellodi C, Landry DM, Niederer RO, Meskauskas A, Musalgaonkar S, et al. rRNA pseudouridylation defects affect ribosomal ligand binding and translational fidelity from yeast to human cells. Molecular cell. 2011 Nov 18;44(4):660–6. doi: 10.1016/j.molcel.2011.09.017 22099312

27. Yoon A, Peng G, Brandenburger Y, Zollo O, Xu W, Rego E, et al. Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science. 2006 May 12;312(5775):902–6. 16690864

28. Preti M, Ribeyre C, Pascali C, Bosio MC, Cortelazzi B, Rougemont J, et al. The telomere-binding protein Tbf1 demarcates snoRNA gene promoters in Saccharomyces cerevisiae. Molecular cell. 2010 May 28;38(4):614–20. doi: 10.1016/j.molcel.2010.04.016 20513435

29. Sheldon KE, Mauger DM, Arndt KM. A Requirement for the Saccharomyces cerevisiae Paf1 complex in snoRNA 3' end formation. Molecular cell. 2005 Oct 28;20(2):225–36. 16246725

30. Simic R, Lindstrom DL, Tran HG, Roinick KL, Costa PJ, Johnson AD, et al. Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes. The EMBO journal. 2003 Apr 15;22(8):1846–56. 12682017

31. Krogan NJ, Kim M, Ahn SH, Zhong G, Kobor MS, Cagney G, et al. RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Molecular and cellular biology. 2002 Oct;22(20):6979–92. 12242279

32. Tomson BN, Crisucci EM, Heisler LE, Gebbia M, Nislow C, Arndt KM. Effects of the Paf1 complex and histone modifications on snoRNA 3'-end formation reveal broad and locus-specific regulation. Molecular and cellular biology. 2013 Jan;33(1):170–82. doi: 10.1128/MCB.01233-12 23109428

33. Landry DM, Hertz MI, Thompson SR. RPS25 is essential for translation initiation by the Dicistroviridae and hepatitis C viral IRESs. Genes & development. 2009 Dec 1;23(23):2753–64.

34. Dinman JD, Kinzy TG. Translational misreading: mutations in translation elongation factor 1alpha differentially affect programmed ribosomal frameshifting and drug sensitivity. Rna. 1997 Aug;3(8):870–81. 9257646

35. Dinman JD, Ruiz-Echevarria MJ, Czaplinski K, Peltz SW. Peptidyl-transferase inhibitors have antiviral properties by altering programmed -1 ribosomal frameshifting efficiencies: development of model systems. Proceedings of the National Academy of Sciences of the United States of America. 1997 Jun 24;94(13):6606–11. 9192612

36. Cui Y, Dinman JD, Kinzy TG, Peltz SW. The Mof2/Sui1 protein is a general monitor of translational accuracy. Molecular and cellular biology. 1998 Mar;18(3):1506–16. 9488467

37. Vicens Q, Westhof E. Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A site. Structure. 2001 Aug;9(8):647–58. 11587639

38. Zuin J, Franke V, van Ijcken WF, van der Sloot A, Krantz ID, van der Reijden MI, et al. A cohesin-independent role for NIPBL at promoters provides insights in CdLS. PLoS genetics. 2014 Feb;10(2):e1004153. doi: 10.1371/journal.pgen.1004153 24550742

39. Mueller CL, Porter SE, Hoffman MG, Jaehning JA. The Paf1 complex has functions independent of actively transcribing RNA polymerase II. Molecular cell. 2004 May 21;14(4):447–56. 15149594

40. Jaehning JA. The Paf1 complex: platform or player in RNA polymerase II transcription? Biochimica et biophysica acta. 2010 May-Jun;1799(5–6):379–88. doi: 10.1016/j.bbagrm.2010.01.001 20060942

41. Chaudhary K, Deb S, Moniaux N, Ponnusamy MP, Batra SK. Human RNA polymerase II-associated factor complex: dysregulation in cancer. Oncogene. 2007 Nov 29;26(54):7499–507. 17599057

42. Xu B, Lee KK, Zhang L, Gerton JL. Stimulation of mTORC1 with L-leucine rescues defects associated with Roberts syndrome. PLoS genetics. 2013;9(10):e1003857. doi: 10.1371/journal.pgen.1003857 24098154

43. Dokal I. Dyskeratosis congenita in all its forms. British journal of haematology. 2000 Sep;110(4):768–79. 11054058

44. Bellodi C, McMahon M, Contreras A, Juliano D, Kopmar N, Nakamura T, et al. H/ACA small RNA dysfunctions in disease reveal key roles for noncoding RNA modifications in hematopoietic stem cell differentiation. Cell reports. 2013 May 30;3(5):1493–502. doi: 10.1016/j.celrep.2013.04.030 23707062

45. Snyder M, Huang XY, Zhang JJ. The minichromosome maintenance proteins 2–7 (MCM2-7) are necessary for RNA polymerase II (Pol II)-mediated transcription. The Journal of biological chemistry. 2009 May 15;284(20):13466–72. doi: 10.1074/jbc.M809471200 19318354

46. Kang HA, Hershey JW. Effect of initiation factor eIF-5A depletion on protein synthesis and proliferation of Saccharomyces cerevisiae. The Journal of biological chemistry. 1994 Feb 11;269(6):3934–40. 8307948

47. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome biology. 2009;10(3):R25. doi: 10.1186/gb-2009-10-3-r25 19261174

48. Glynn EF, Megee PC, Yu HG, Mistrot C, Unal E, Koshland DE, et al. Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS biology. 2004 Sep;2(9):E259. 15309048

49. Deniz N, Lenarcic EM, Landry DM, Thompson SR. Translation initiation factors are not required for Dicistroviridae IRES function in vivo. Rna. 2009 May;15(5):932–46. doi: 10.1261/rna.1315109 19299549

50. Harger JW, Dinman JD. An in vivo dual-luciferase assay system for studying translational recoding in the yeast Saccharomyces cerevisiae. Rna. 2003 Aug;9(8):1019–24. 12869712

51. Grentzmann G, Ingram JA, Kelly PJ, Gesteland RF, Atkins JF. A dual-luciferase reporter system for studying recoding signals. Rna. 1998 Apr;4(4):479–86. 9630253

52. Kim DH, Koepp DM. Hect E3 ubiquitin ligase Tom1 controls Dia2 degradation during the cell cycle. Molecular biology of the cell. 2012 Nov;23(21):4203–11. doi: 10.1091/mbc.E12-07-0548 22933573

53. Kim DH, Zhang W, Koepp DM. The Hect domain E3 ligase Tom1 and the F-box protein Dia2 control Cdc6 degradation in G1 phase. The Journal of biological chemistry. 2012 Dec 28;287(53):44212–20. doi: 10.1074/jbc.M112.401778 23129771

54. Bakin A, Ofengand J. Four newly located pseudouridylate residues in Escherichia coli 23S ribosomal RNA are all at the peptidyltransferase center: analysis by the application of a new sequencing technique. Biochemistry. 1993 Sep 21;32(37):9754–62. 8373778

55. Ganot P, Bortolin ML, Kiss T. Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell. 1997 May 30;89(5):799–809. 9182768

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 7
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#