INO80 Chromatin Remodeler Facilitates Release of RNA Polymerase II from Chromatin for Ubiquitin-Mediated Proteasomal Degradation

Molecular Cell

Volumn 60, Issue 5, 2015, Pages 784-796

  Lafon, Anne ^a   Taranum, Surayya ^a   Pietrocola, Federico ^a   Dingli, Florent ^b   Loew, Damarys ^b   Brahma, Sandipan ^c   Bartholomew, Blaine ^c   Papamichos Chronakis, Manolis ^a  

^a INSTITUT CURIE   (France)

^b INSTITUT CURIE   (France)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CDC48 PROTEIN; INO80 PROTEIN; PROTEASOME; PROTEIN P97; RNA POLYMERASE II; RPB1 PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CHROMATIN; INO80 COMPLEX, S CEREVISIAE; RPB1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL GROWTH; CELL SURVIVAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPLEX FORMATION; CONTROLLED STUDY; DISSOCIATION; GENOME; GENOTOXICITY; NONHUMAN; NUCLEOSOME; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; YEAST; CHROMATIN; FUNGAL GENOME; GENETICS; METABOLISM; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATASES; CELL CYCLE PROTEINS; CHROMATIN; GENOME, FUNGAL; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITINATION;

EID: 84952870053     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.10.028     Document Type: Article

References (55)

1. Aguilera A., García-Muse T. Causes of genome instability. Annu. Rev. Genet. 2013, 47:1-32.
2. Allen J.B., Zhou Z., Siede W., Friedberg E.C., Elledge S.J. The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev. 1994, 8:2401-2415.
3. Anindya R., Aygün O., Svejstrup J.Q. Damage-induced ubiquitylation of human RNA polymerase II by the ubiquitin ligase Nedd4, but not Cockayne syndrome proteins or BRCA1. Mol. Cell 2007, 28:386-397.
4. Auld K.L., Brown C.R., Casolari J.M., Komili S., Silver P.A. Genomic association of the proteasome demonstrates overlapping gene regulatory activity with transcription factor substrates. Mol. Cell 2006, 21:861-871.
5. Bartholomew B. Regulating the chromatin landscape: structural and mechanistic perspectives. Annu. Rev. Biochem. 2014, 83:671-696.
6. Beaudenon S.L., Huacani M.R., Wang G., McDonnell D.P., Huibregtse J.M. Rsp5 ubiquitin-protein ligase mediates DNA damage-induced degradation of the large subunit of RNA polymerase II in Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19:6972-6979.
7. Becuwe M., Vieira N., Lara D., Gomes-Rezende J., Soares-Cunha C., Casal M., Haguenauer-Tsapis R., Vincent O., Paiva S., Léon S. A molecular switch on an arrestin-like protein relays glucose signaling to transporter endocytosis. J. Cell Biol. 2012, 196:247-259.
8. Bintu L., Ishibashi T., Dangkulwanich M., Wu Y.Y., Lubkowska L., Kashlev M., Bustamante C. Nucleosomal elements that control the topography of the barrier to transcription. Cell 2012, 151:738-749.
9. Bondarenko V.A., Steele L.M., Ujvári A., Gaykalova D.A., Kulaeva O.I., Polikanov Y.S., Luse D.S., Studitsky V.M. Nucleosomes can form a polar barrier to transcript elongation by RNA polymerase II. Mol. Cell 2006, 24:469-479.
10. Buckley S.M., Aranda-Orgilles B., Strikoudis A., Apostolou E., Loizou E., Moran-Crusio K., Farnsworth C.L., Koller A.A., Dasgupta R., Silva J.C., et al. Regulation of pluripotency and cellular reprogramming by the ubiquitin-proteasome system. Cell Stem Cell 2012, 11:783-798.
11. Chang H.W., Kulaeva O.I., Shaytan A.K., Kibanov M., Kuznedelov K., Severinov K.V., Kirpichnikov M.P., Clark D.J., Studitsky V.M. Analysis of the mechanism of nucleosome survival during transcription. Nucleic Acids Res. 2014, 42:1619-1627.
12. Charlet-Berguerand N., Feuerhahn S., Kong S.E., Ziserman H., Conaway J.W., Conaway R., Egly J.M. RNA polymerase II bypass of oxidative DNA damage is regulated by transcription elongation factors. EMBO J. 2006, 25:5481-5491.
13. Churchman L.S., Weissman J.S. Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature 2011, 469:368-373.
14. Clapier C.R., Cairns B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 2009, 78:273-304.
15. Conaway R.C., Conaway J.W. The INO80 chromatin remodeling complex in transcription, replication and repair. Trends Biochem. Sci. 2009, 34:71-77.
16. Daulny A., Tansey W.P. Damage control: DNA repair, transcription, and the ubiquitin-proteasome system. DNA Repair (Amst.) 2009, 8:444-448.
17. Decottignies A., Evain A., Ghislain M. Binding of Cdc48p to a ubiquitin-related UBX domain from novel yeast proteins involved in intracellular proteolysis and sporulation. Yeast 2004, 21:127-139.
18. Haffner M.C., De Marzo A.M., Meeker A.K., Nelson W.G., Yegnasubramanian S. Transcription-induced DNA double strand breaks: both oncogenic force and potential therapeutic target?. Clin. Cancer Res. 2011, 17:3858-3864.
19. Helmrich A., Ballarino M., Nudler E., Tora L. Transcription-replication encounters, consequences and genomic instability. Nat. Struct. Mol. Biol. 2013, 20:412-418.
20. Huibregtse J.M., Yang J.C., Beaudenon S.L. The large subunit of RNA polymerase II is a substrate of the Rsp5 ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA 1997, 94:3656-3661.
21. Jentsch S., Rumpf S. Cdc48 (p97): a "molecular gearbox" in the ubiquitin pathway?. Trends Biochem. Sci. 2007, 32:6-11.
22. Jin J., Cai Y., Yao T., Gottschalk A.J., Florens L., Swanson S.K., Gutiérrez J.L., Coleman M.K., Workman J.L., Mushegian A., et al. A mammalian chromatin remodeling complex with similarities to the yeast INO80 complex. J. Biol. Chem. 2005, 280:41207-41212.
23. Jónsson Z.O., Jha S., Wohlschlegel J.A., Dutta A. Rvb1p/Rvb2p recruit Arp5p and assemble a functional Ino80 chromatin remodeling complex. Mol. Cell 2004, 16:465-477.
24. Kikuchi M., Ogishima S., Miyamoto T., Miyashita A., Kuwano R., Nakaya J., Tanaka H. Identification of unstable network modules reveals disease modules associated with the progression of Alzheimer's disease. PLoS ONE 2013, 8:e76162.
25. Longtine M.S., McKenzie A., Demarini D.J., Shah N.G., Wach A., Brachat A., Philippsen P., Pringle J.R. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998, 14:953-961.
26. Meyer H., Bug M., Bremer S. Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system. Nat. Cell Biol. 2012, 14:117-123.
27. Pankotai T., Bonhomme C., Chen D., Soutoglou E. DNAPKcs-dependent arrest of RNA polymerase II transcription in the presence of DNA breaks. Nat. Struct. Mol. Biol. 2012, 19:276-282.
28. Papamichos-Chronakis M., Peterson C.L. The Ino80 chromatin-remodeling enzyme regulates replisome function and stability. Nat. Struct. Mol. Biol. 2008, 15:338-345.
29. Papamichos-Chronakis M., Watanabe S., Rando O.J., Peterson C.L. Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 2011, 144:200-213.
30. Pellicioli A., Lucca C., Liberi G., Marini F., Lopes M., Plevani P., Romano A., Di Fiore P.P., Foiani M. Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J. 1999, 18:6561-6572.
31. Piñeiro M., Puerta C., Palacián E. Yeast nucleosomal particles: structural and transcriptional properties. Biochemistry 1991, 30:5805-5810.
32. Ramotar D., Wang H. Protective mechanisms against the antitumor agent bleomycin: lessons from Saccharomyces cerevisiae. Curr. Genet. 2003, 43:213-224.
33. Ray S., Grove A. Interaction of Saccharomyces cerevisiae HMO2 domains with distorted DNA. Biochemistry 2012, 51:1825-1835.
34. Ribar B., Prakash L., Prakash S. ELA1 and CUL3 are required along with ELC1 for RNA polymerase II polyubiquitylation and degradation in DNA-damaged yeast cells. Mol. Cell. Biol. 2007, 27:3211-3216.
35. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 1998, 273:5858-5868.
36. Saha A., Wittmeyer J., Cairns B.R. Chromatin remodelling: the industrial revolution of DNA around histones. Nat. Rev. Mol. Cell Biol. 2006, 7:437-447.
37. Sarkar S., Kiely R., McHugh P.J. The Ino80 chromatin-remodeling complex restores chromatin structure during UV DNA damage repair. J. Cell Biol. 2010, 191:1061-1068.
38. Schuberth C., Buchberger A. UBX domain proteins: major regulators of the AAA ATPase Cdc48/p97. Cell. Mol. Life Sci. 2008, 65:2360-2371.
39. Selby C.P., Sancar A. Molecular mechanism of transcription-repair coupling. Science 1993, 260:53-58.
40. Selby C.P., Sancar A. Human transcription-repair coupling factor CSB/ERCC6 is a DNA-stimulated ATPase but is not a helicase and does not disrupt the ternary transcription complex of stalled RNA polymerase II. J. Biol. Chem. 1997, 272:1885-1890.
41. Shen X., Ranallo R., Choi E., Wu C. Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol. Cell 2003, 12:147-155.
42. Sinha M., Watanabe S., Johnson A., Moazed D., Peterson C.L. Recombinational repair within heterochromatin requires ATP-dependent chromatin remodeling. Cell 2009, 138:1109-1121.
43. Somesh B.P., Reid J., Liu W.F., Søgaard T.M., Erdjument-Bromage H., Tempst P., Svejstrup J.Q. Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest. Cell 2005, 121:913-923.
44. Somesh B.P., Sigurdsson S., Saeki H., Erdjument-Bromage H., Tempst P., Svejstrup J.Q. Communication between distant sites in RNA polymerase II through ubiquitylation factors and the polymerase CTD. Cell 2007, 129:57-68.
45. Svejstrup J.Q. Contending with transcriptional arrest during RNAPII transcript elongation. Trends Biochem. Sci. 2007, 32:165-171.
46. Tercero J.A., Longhese M.P., Diffley J.F. A central role for DNA replication forks in checkpoint activation and response. Mol. Cell 2003, 11:1323-1336.
47. Tosi A., Haas C., Herzog F., Gilmozzi A., Berninghausen O., Ungewickell C., Gerhold C.B., Lakomek K., Aebersold R., Beckmann R., Hopfner K.P. Structure and subunit topology of the INO80 chromatin remodeler and its nucleosome complex. Cell 2013, 154:1207-1219.
48. Udugama M., Sabri A., Bartholomew B. The INO80 ATP-dependent chromatin remodeling complex is a nucleosome spacing factor. Mol. Cell. Biol. 2011, 31:662-673.
49. Verma R., Oania R., Fang R., Smith G.T., Deshaies R.J. Cdc48/p97 mediates UV-dependent turnover of RNA Pol II. Mol. Cell 2011, 41:82-92.
50. Wang L., Du Y., Ward J.M., Shimbo T., Lackford B., Zheng X., Miao Y.L., Zhou B., Han L., Fargo D.C., et al. INO80 facilitates pluripotency gene activation in embryonic stem cell self-renewal, reprogramming, and blastocyst development. Cell Stem Cell 2014, 14:575-591.
51. Wilson M.D., Harreman M., Svejstrup J.Q. Ubiquitylation and degradation of elongating RNA polymerase II: the last resort. Biochim. Biophys. Acta 2013, 1829:151-157.
52. Woudstra E.C., Gilbert C., Fellows J., Jansen L., Brouwer J., Erdjument-Bromage H., Tempst P., Svejstrup J.Q. A Rad26-Def1 complex coordinates repair and RNA pol II proteolysis in response to DNA damage. Nature 2002, 415:929-933.
53. Yao T., Song L., Jin J., Cai Y., Takahashi H., Swanson S.K., Washburn M.P., Florens L., Conaway R.C., Cohen R.E., Conaway J.W. Distinct modes of regulation of the Uch37 deubiquitinating enzyme in the proteasome and in the Ino80 chromatin-remodeling complex. Mol. Cell 2008, 31:909-917.
54. Yen K., Vinayachandran V., Batta K., Koerber R.T., Pugh B.F. Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell 2012, 149:1461-1473.
55. Yen K., Vinayachandran V., Pugh B.F. SWR-C and INO80 chromatin remodelers recognize nucleosome-free regions near +1 nucleosomes. Cell 2013, 154:1246-1256.