Senataxin controls meiotic silencing through ATR activation and chromatin remodeling

Cell Discovery

Volumn 1, Issue , 2015, Pages

  Yeo, Abrey J ^a   Becherel, Olivier J ^a   Luff, John E ^a   Graham, Mark E ^b   Richard, Derek ^c   Lavin, Martin F ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

chromatin remodeling; DNA damage repair; meiosis; Senataxin; transcription

Indexed keywords

ATR PROTEIN; CHROMODOMAIN HELICASE DNA BINDING PROTEIN 4; DNA BINDING PROTEIN; HELICASE; HISTONE; SENATAXIN; TOPBP1 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; GENE ACTIVATION; GENE DISRUPTION; HISTONE ACETYLATION; MALE; MEIOSIS; MOUSE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPERMATOCYTE; SUMOYLATION; TRANSCRIPTION TERMINATION; X CHROMOSOME; Y CHROMOSOME;

EID: 84994872534     PISSN: None     EISSN: 20565968     Source Type: Journal    
DOI: 10.1038/celldisc.2015.25     Document Type: Article

References (61)

1. Anheim M, Monga B, Fleury M et al. Ataxia with oculomotor apraxia type 2: clinical, biological and genotype/phenotype correlation study of a cohort of 90 patients. Brain 2009; 132: 2688-2698.
2. Moreira MC, Klur S, Watanabe M et al. Senataxin, the ortholog of a yeast RNA helicase, is mutant in ataxia-ocular apraxia 2. Nat Genet 2004; 36: 225-227.
3. Chen YZ, Bennett CL, Huynh HM et al. DNA/RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (ALS4). Am J Hum Genet 2004; 74: 1128-1135.
4. Hirano M, Quinzii CM, Mitsumoto H et al. Senataxin mutations and amyotrophic lateral sclerosis. Amyotroph Lateral Sc 2011; 12: 223-227.
5. Richard P, Feng S, Manley JL. A SUMO-dependent interaction between Senataxin and the exosome, disrupted in the neurodegenerative disease AOA2, targets the exosome to sites of transcription-induced DNA damage. Gene Dev 2013; 27: 2227-2232.
6. Kim M, Vasiljeva L, Rando OJ, Zhelkovsky A, Moore C, Buratowski S. Distinct pathways for snoRNA and mRNA termination. Mol Cell 2006; 24: 723-734.
7. Steinmetz EJ, Warren CL, Kuehner JN, Panbehi B, Ansari AZ, Brow DA. Genome-wide distribution of yeast RNA polymerase II and its control by Sen1 helicase. Mol Cell 2006; 24: 735-746.
8. Ursic D, Chinchilla K, Finkel JS, Culbertson MR. Multiple protein/protein and protein/RNA interactions suggest roles for yeast DNA/RNA helicase Sen1p in transcription, transcription-coupled DNA repair and RNA processing. Nucleic Acids Res 2004; 32: 2441-2452.
9. De Amicis A, Piane M, Ferrari F, Fanciulli M, Delia D, Chessa L. Role of senataxin in DNA damage and telomeric stability. DNA Rep 2011; 10: 199-209.
10. Lavin MF. The appropriateness of the mouse model for ataxia-telangiectasia: neurological defects but no neurodegeneration. DNA Rep 2013; 12: 612-619.
11. Suraweera A, Becherel OJ, Chen P et al. Senataxin, defective in ataxia oculomotor apraxia type 2, is involved in the defense against oxidative DNA damage. J Cell Biol 2007; 177: 969-979.
12. Suraweera A, Lim Y, Woods R et al. Functional role for senataxin, defective in ataxia oculomotor apraxia type 2, in transcriptional regulation. Hum Mol Genet 2009; 18: 3384-3396.
13. Skourti-Stathaki K, Proudfoot NJ, Gromak N. Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. Mol Cell 2011; 42: 794-805.
14. Mischo HE, Gomez-Gonzalez B, Grzechnik P et al. Yeast Sen1 helicase protects the genome from transcriptionassociated instability. Mol Cell 2011; 41: 21-32.
15. Aguilera A, Gomez-Gonzalez B. Genome instability: a mechanistic view of its causes and consequences. Nat Rev Genet 2008; 9: 204-217.
16. Yuce O, West SC. Senataxin, defective in the neurodegenerative disorder ataxia with oculomotor apraxia 2, lies at the interface of transcription and the DNA damage response. Mol Cell Biol 2013; 33: 406-417.
17. Alzu A, Bermejo R, Begnis M et al. Senataxin associates with replication forks to protect fork integrity across RNApolymerase-II-transcribed genes. Cell 2012; 151: 835-846.
18. Miller MS, Rialdi A, Ho JS et al. Senataxin suppresses the antiviral transcriptional response and controls viral biogenesis. Nat Immunol 2015; 16: 485-494.
19. Yeo AJ, Becherel OJ, Luff JE et al. R-loops in proliferating cells but not in the brain: implications for AOA2 and other autosomal recessive ataxias. PLoS ONE 2014; 9: e90219.
20. Becherel OJ, Yeo AJ, Stellati et al. Senataxin plays an essential role with DNA damage response proteins in meiotic recombination and gene silencing. PLoS Genet 2013; 9: e1003435.
21. Yuan L, Liu JG, Zhao J, Brundell E, Daneholt B, Hoog C. The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol Cell 2000; 5: 73-83.
22. Hecker CM, Rabiller M, Haglund K, Bayer P, Dikic I. Specification of SUMO1-and SUMO2-interacting motifs. J Biol Chem 2006; 281: 16117-16127.
23. Raman N, Nayak A, Muller S. The SUMO system: a master organizer of nuclear protein assemblies. Chromosoma 2013; 122: 475-485.
24. Vigodner M. Sumoylation precedes accumulation of phosphorylated H2AX on sex chromosomes during their meiotic inactivation. Chromosome Res 2009; 17: 37-45.
25. Turner JM, Aprelikova O, Xu X et al. BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr Biol 2004; 14: 2135-2142.
26. Namiki Y, Zou L. ATRIP associates with replication protein A-coated ssDNA through multiple interactions. Proc Natl Acad Sci USA 2006; 103: 580-585.
27. Shiotani B, Zou L. ATR signaling at a glance. J Cell Sci 2009; 122: 301-304.
28. Zou L, Elledge SJ. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003; 300: 1542-1548.
29. Fernandez-Capetillo O, Mahadevaiah SK, Celeste et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 2003; 4: 497-508.
30. Daniel K, Lange J, Hached K et al. Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat Cell Biol 2011; 13: 599-U232.
31. Liu SQ, Opiyo SO, Manthey K et al. Distinct roles for DNA-PK, ATM and ATR in RPA phosphorylation and checkpoint activation in response to replication stress. Nucleic Acids Res 2012; 40: 10780-10794.
32. Yilmaz S, Sancar A, Kemp MG. Multiple ATR-Chk1 pathway proteins preferentially associate with checkpointinducing DNA substrates. PLoS Ine 2011; 6: e22986.
33. Cha RS, Kleckner N. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 2002; 297: 602-606.
34. Sorensen CS, Syljuasen RG. Safeguarding genome integrity: the checkpoint kinases ATR, CHK1 and WEE1 restrain CDK activity during normal DNA replication. Nucleic Acids Res 2012; 40: 477-486.
35. Liu S, Ho CK, Ouyang J, Zou L. Nek1 kinase associates with ATR-ATRIP and primes ATR for efficient DNA damage signaling. Proc Natl Acad Sci USA 2013; 110: 2175-2180.
36. Xue YT, Wong JM, Moreno GT, Young MK, Cote J, Wang WD. NURD, a novel complex with both ATPdependent chromatin-remodeling and histone deacetylase activities. Mol Cell 1998; 2: 851-861.
37. McArt DG, Zhang SD. Identification of candidate smallmolecule therapeutics to cancer by gene-signature perturbation in connectivity mapping. PLoS ONE 2011; 6: e16382.
38. Schmidt DR, Schreiber SL. Molecular association between ATR and two components of the nucleosome remodeling and deacetylating complex, HDAC2 and CHD4. Biochemistry-Us 1999; 38: 14711-14717.
39. Urquhart AJ, Gatei M, Richard DJ, Khanna KK. ATM mediated phosphorylation of CHD4 contributes to genome maintenance. Genome Integr 2011; 2: 1.
40. Musselman CA, Ramirez J, Sims JK et al. Bivalent recognition of nucleosomes by the tandem PHD fingers of the CHD4 ATPase is required for CHD4-mediated repression. Proc Natl Acad Sci USA 2012; 109: 787-792.
41. Morris SA, Baek S, Sung MH et al. Overlapping chromatin-remodeling systems collaborate genome wide at dynamic chromatin transitions. (vol 21, pg 73, 2014). Nat Struct Mol Biol 2014; 21: 1106-1106.
42. Page J, de la Fuente R, Manterola M et al. Inactivation or non-reactivation: what accounts better for the silence of sex chromosomes during mammalian male meiosis? Chromosoma 2012; 121: 307-326.
43. Ginno PA, Lott PL, Christensen HC,Korf I, Chedin F. R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol Cell 2012; 45: 814-825.
44. Zhang Y, Reinberg D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 2001; 15: 2343-2360.
45. An W. Histone acetylation and methylation: combinatorial players for transcriptional regulation. Subcell Biochem 2007; 41: 351-369.
46. Ramirez J, Dege C, Kutateladze TG, Hagman J. MBD2 and multiple domains of CHD4 are required for transcriptional repression by Mi-2/NuRD complexes. Mol Cell Biol 2012; 32: 5078-5088.
47. Royo H, Prosser H, Ruzankina Y et al. ATR acts stage specifically to regulate multiple aspects of mammalian meiotic silencing. Gene Dev 2013; 27: 1484-1494.
48. Nam EA, Cortez D. AIR signalling: more than meeting at the fork. Biochem J 2011; 436: 527-536.
49. Zeman MK, Cimprich KA. Causes and consequences of replication stress. Nat Cell Biol 2014; 16: 2-9.
50. Refolio E, Cavero S, Marcon E, Freire R, San-Segundo PA. The Ddc2/ATRIP checkpoint protein monitors meiotic recombination intermediates. J Cell Sci 2011; 124: 2488-2500.
51. Wu CS, Ouyang J, Mori E et al. SUMOylation of ATRIP potentiates DNA damage signaling by boosting multiple protein interactions in the ATR pathway. Gene Dev 2014; 28: 1472-1484.
52. Xiao Z, Chang JG, Hendriks IA, Sigurethsson JO, Olsen JV, Vertegaal AC. System-wide analysis of SUMOylation dynamics in response to replication stress reveals novel small ubiquitin-like modified target proteins and acceptor lysines relevant for genome stability. Mol Cell Proteom 2015; 14: 1419-1434.
53. Levy MA, Kernohan KD, Jiang Y, Berube NG. ATRX promotes gene expression by facilitating transcriptional elongation through guanine-rich coding regions. Hum Mol Genet 2014; 24: 1824-1835.
54. Haeusler AR, Donnelly CJ, Periz G et al. C9orf72 nucleotide repeat structures initiate molecular cascades of disease. Nature 2014; 507: 195-200.
55. Mosallanejad K, Sekine Y, Ishikura-Kinoshita S et al. The DEAH-box RNA helicase DHX15 activates NF-kappaB and MAPK signaling downstream of MAVS during antiviral responses. Sci Signal 2014; 7: 40.
56. Magalska A, Schellhaus AK, Moreno-Andres D et al. RuvB-like ATPases function in chromatin decondensation at the end of mitosis. Dev Cell 2014; 31: 305-318.
57. Ahringer J. NuRD and SIN3 histone deacetylase complexes in development. Trends Genet 2000; 16: 351-356.
58. O'Shaughnessy A, Hendrich B. CHD4 in the DNA-damage response and cell cycle progression: not so NuRDy now. Biochem Soc Trans 2013; 41: 777-782.
59. Larsen DH, Poinsignon C, Gudjonsson T et al. The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J Cell Biol 2010; 190: 731-740.
60. Cheng J, Blum R, Bowman C et al. A role for H3K4 monomethylation in gene repression and partitioning of chromatin readers. Mol Cell 2014; 53: 979-992.
61. Sollier J, Stork CT, Garcia-Rubio ML, Paulsen RD, Aguilera A, Cimprich KA. Transcription-coupled nucleotide excision repair factors promote R-loop-induced genome instability. Mol cell 2014; 56: 777-785.