Activation of a novel ubiquitin-independent proteasome pathway when RNA polymerase II encounters a protein roadblock

Molecular and Cellular Biology

Volumn 33, Issue 20, 2013, Pages 4008-4016

  Ban, Yi ^a   Ho, Chia Wen ^a   Lin, Ren Kuo ^a   Lyu, Yi Lisa ^a   Liu, Leroy F ^a,b  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DNA TOPOISOMERASE; ETOPOSIDE; PROTEASOME; RNA POLYMERASE II; SMALL INTERFERING RNA; TOPOISOMERASE 2BETA; UBIQUITIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; COMPLEX FORMATION; FIBROBLAST; GENE SILENCING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION ELONGATION;

ADENOSINE TRIPHOSPHATASES; ANIMALS; DNA; DNA REPAIR; DNA TOPOISOMERASES, TYPE II; DNA-BINDING PROTEINS; EMBRYO, MAMMALIAN; FIBROBLASTS; HELA CELLS; HUMANS; MICE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; RNA POLYMERASE II; TRANSCRIPTION ELONGATION, GENETIC; UBIQUITIN;

EID: 84886878906     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00403-13     Document Type: Article

References (50)

1. Ratner JN, Balasubramanian B, Corden J, Warren SL, Bregman DB. 1998. Ultraviolet radiation-induced ubiquitination and proteasomal degradation of the large subunit of RNA polymerase II. Implications for transcription-coupled DNA repair. J. Biol. Chem. 273:5184-5189.
2. Svejstrup JQ. 2007. Contending with transcriptional arrest during RNAPII transcript elongation. Trends Biochem. Sci. 32:165-171.
3. Anindya R, Aygun O, Svejstrup JQ. 2007. Damage-induced ubiquitylation of human RNA polymerase II by the ubiquitin ligase Nedd4, but not Cockayne syndrome proteins or BRCA1. Mol. Cell 28:386-397.
4. Luo Z, Zheng J, Lu Y, Bregman DB. 2001. Ultraviolet radiation alters the phosphorylation of RNA polymerase II large subunit and accelerates its proteasome-dependent degradation. Mutat. Res. 486:259-274.
5. Dahmus ME. 1995. Phosphorylation of the C-terminal domain of RNA polymerase II. Biochim. Biophys. Acta 1261:171-182.
6. Harreman M, Taschner M, Sigurdsson S, Anindya R, Reid J, Somesh B, Kong SE, Banks CA, Conaway RC, Conaway JW, Svejstrup JQ. 2009. Distinct ubiquitin ligases act sequentially for RNA polymerase II polyubiquitylation. Proc. Natl. Acad. Sci. U. S. A. 106:20705-20710.
7. Somesh BP, Reid J, Liu WF, Sogaard TM, Erdjument-Bromage H, Tempst P, Svejstrup JQ. 2005. Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest. Cell 121:913-923.
8. Mao Y, Desai SD, Ting CY, Hwang J, Liu LF. 2001. 26S proteasomemediated degradation of topoisomerase II cleavable complexes. J. Biol. Chem. 276:40652-40658.
9. Zhang A, Lyu YL, Lin CP, Zhou N, Azarova AM, Wood LM, Liu LF. 2006.Aprotease pathway for the repair of topoisomerase II-DNA covalent complexes. J. Biol. Chem. 281:35997-36003.
10. Azarova AM, Lyu YL, Lin CP, Tsai YC, Lau JY, Wang JC, Liu LF. 2007. Roles of DNA topoisomerase II isozymes in chemotherapy and secondary malignancies. Proc. Natl. Acad. Sci. U. S. A. 104:11014-11019.
11. Lyu YL, Kerrigan JE, Lin CP, Azarova AM, Tsai YC, Ban Y, Liu LF. 2007. Topoisomerase IIbeta mediated DNA double-strand breaks: implications in doxorubicin cardiotoxicity and prevention by dexrazoxane. Cancer Res. 67:8839-8846.
12. Zhang S, Liu X, Bawa-Khalfe T, Lu LS, Lyu YL, Liu LF, Yeh ET. 2012. Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat. Med. 18:1639-1642.
13. Gonzalez F, Delahodde A, Kodadek T, Johnston SA. 2002. Recruitment of a 19S proteasome subcomplex to an activated promoter. Science 296: 548-550.
14. Ferdous A, Kodadek T, Johnston SA. 2002. A nonproteolytic function of the 19S regulatory subunit of the 26S proteasome is required for efficient activated transcription by human RNA polymerase II. Biochemistry 41: 12798-12805.
15. Gillette TG, Gonzalez F, Delahodde A, Johnston SA, Kodadek T. 2004. Physical and functional association of RNA polymerase II and the proteasome. Proc. Natl. Acad. Sci. U. S. A. 101:5904-5909.
16. Muratani M, Tansey WP. 2003. How the ubiquitin-proteasome system controls transcription. Nat. Rev. Mol. Cell Biol. 4:192-201.
17. Shero JH, Bordwell B, Rothfield NF, Earnshaw WC. 1986. High titers of autoantibodies to topoisomerase I (Scl-70) in sera from scleroderma patients. Science 231:737-740.
18. Desai SD, Li TK, Rodriguez-Bauman A, Rubin EH, Liu LF. 2001. Ubiquitin/26S proteasome-mediated degradation of topoisomerase I as a resistance mechanism to camptothecin in tumor cells. Cancer Res. 61: 5926-5932.
19. Mayer A, Gropper R, Schwartz AL, Ciechanover A. 1989. Purification, characterization, and rapid inactivation of thermolabile ubiquitinactivating enzyme from the mammalian cell cycle mutant ts85. J. Biol. Chem. 264:2060-2068.
20. Lin CP, Ban Y, Lyu YL, Desai SD, Liu LF. 2008. A ubiquitin-proteasome pathway for the repair of topoisomerase I-DNA covalent complexes. J. Biol. Chem. 283:21074-21083.
21. Smith DM, Chang SC, Park S, Finley D, Cheng Y, Goldberg AL. 2007. Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's alpha ring opens the gate for substrate entry. Mol. Cell 27:731-744.
22. Howl J, Jones S. 2009. Transport molecules using reverse sequence HIVTat polypeptides: not just any old Tat? (WO200808225). Expert Opin. Ther. Pat. 19:1329-1333.
23. Abes S, Moulton H, Turner J, Clair P, Richard JP, Iversen P, Gait MJ, Lebleu B. 2007. Peptide-based delivery of nucleic acids: design, mechanism of uptake and applications to splice-correcting oligonucleotides. Biochem. Soc. Trans. 35:53-55.
24. Yamaguchi Y, Wada T, Handa H. 1998. Interplay between positive and negative elongation factors: drawing a new view of DRB. Genes Cells 3:9-15.
25. Meinhart A, Cramer P. 2004. Recognition of RNA polymerase II carboxy-terminal domain by 3=-RNA-processing factors. Nature 430:223-226.
26. Cadena DL, Dahmus ME. 1987. Messenger RNA synthesis in mammalian cells is catalyzed by the phosphorylated form ofRNApolymerase II. J. Biol. Chem. 262:12468-12474.
27. Payne JM, Laybourn PJ, Dahmus ME. 1989. The transition of RNA polymerase II from initiation to elongation is associated with phosphorylation of the carboxyl-terminal domain of subunit IIa. J. Biol. Chem. 264: 19621-19629.
28. Christensen MO, Larsen MK, Barthelmes HU, Hock R, Andersen CL, Kjeldsen E, Knudsen BR, Westergaard O, Boege F, Mielke C. 2002. Dynamics of human DNA topoisomerases IIalpha and IIbeta in living cells. J. Cell Biol. 157:31-44.
29. Fricke B, Heink S, Steffen J, Kloetzel PM, Kruger E. 2007. The proteasome maturation protein POMP facilitates major steps of 20S proteasome formation at the endoplasmic reticulum. EMBO Rep. 8:1170-1175.
30. Heink S, Ludwig D, Kloetzel PM, Kruger E. 2005. IFN-gamma-induced immune adaptation of the proteasome system is an accelerated and transient response. Proc. Natl. Acad. Sci. U. S. A. 102:9241-9246.
31. Chen X, Chi Y, Bloecher A, Aebersold R, Clurman BE, Roberts JM. 2004. N-acetylation and ubiquitin-independent proteasomal degradation of p21(Cip1). Mol. Cell 16:839-847.
32. Sdek P, Ying H, Chang DL, Qiu W, Zheng H, Touitou R, Allday MJ, Xiao ZX. 2005. MDM2 promotes proteasome-dependent ubiquitinindependent degradation of retinoblastoma protein. Mol. Cell 20:699-s708.
33. Touitou R, Richardson J, Bose S, Nakanishi M, Rivett J, Allday MJ. 2001. A degradation signal located in the C-terminus of p21WAF1/CIP1 is a binding site for the C8 alpha-subunit of the 20S proteasome. EMBO J. 20:2367-2375.
34. Zhang M, Pickart CM, Coffino P. 2003. Determinants of proteasome recognition of ornithine decarboxylase, a ubiquitin-independent substrate. EMBO J. 22:1488-1496.
35. Glockzin S, Ogi FX, Hengstermann A, Scheffner M, Blattner C. 2003. Involvement of the DNA repair protein hHR23 in p53 degradation. Mol. Cell. Biol. 23:8960-8969.
36. Raasi S, Pickart CM. 2003. Rad23 ubiquitin-associated domains (UBA) inhibit 26S proteasome-catalyzed proteolysis by sequestering lysine 48-linked polyubiquitin chains. J. Biol. Chem. 278:8951-8959.
37. Li X, Lonard DM, Jung SY, Malovannaya A, Feng Q, Qin J, Tsai SY, Tsai MJ, O'Malley BW. 2006. The SRC-3/AIB1 coactivator is degraded in a ubiquitin- and ATP-independent manner by the REGgamma proteasome. Cell 124:381-392.
38. Rabl J, Smith DM, Yu Y, Chang SC, Goldberg AL, Cheng Y. 2008. Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol. Cell 30:360-368.
39. Besche HC, Peth A, Goldberg AL. 2009. Getting to first base in proteasome assembly. Cell 138:25-28.
40. Le Tallec B, Barrault MB, Guerois R, Carre T, Peyroche A. 2009. Hsm3/S5b participates in the assembly pathway of the 19S regulatory particle of the proteasome. Mol. Cell 33:389-399.
41. Park S, Roelofs J, Kim W, Robert J, Schmidt M, Gygi SP, Finley D. 2009. Hexameric assembly of the proteasomal ATPases is templated through their C termini. Nature 459:866-870.
42. Roelofs J, Park S, Haas W, Tian G, McAllister FE, Huo Y, Lee BH, Zhang F, Shi Y, Gygi SP, Finley D. 2009. Chaperone-mediated pathway of proteasome regulatory particle assembly. Nature 459:861-865.
43. Kaneko T, Hamazaki J, Iemura S, Sasaki K, Furuyama K, Natsume T, Tanaka K, Murata S. 2009. Assembly pathway of the mammalian proteasome base subcomplex is mediated by multiple specific chaperones. Cell 137:914-925.
44. Felix CA. 1998. Secondary leukemias induced by topoisomerase-targeted drugs. Biochim. Biophys. Acta 1400:233-255.
45. Jacquemont C, Taniguchi T. 2007. Proteasome function is required for DNA damage response and fanconi anemia pathway activation. Cancer Res. 67:7395-7405.
46. Ishizuka T, Satoh T, Monden T, Shibusawa N, Hashida T, Yamada M, Mori M. 2001. Human immunodeficiency virus type 1 Tat binding protein-1 is a transcriptional coactivator specific for TR. Mol. Endocrinol. 15:1329-1343.
47. Satoh T, Ishizuka T, Tomaru T, Yoshino S, Nakajima Y, Hashimoto K, Shibusawa N, Monden T, Yamada M, Mori M. 2009. Tat-binding protein-1 (TBP-1), an ATPase of 19S regulatory particles of the 26S proteasome, enhances androgen receptor function in cooperation with TBP-1-interacting protein/Hop2. Endocrinology 150:3283-3290.
48. Desai SD, Zhang H, Rodriguez-Bauman A, Yang JM, Wu X, Gounder MK, Rubin EH, Liu LF. 2003. Transcription-dependent degradation of topoisomerase I-DNA covalent complexes. Mol. Cell. Biol. 23:2341-2350.
49. Pouliot JJ, Yao KC, Robertson CA, Nash HA. 1999. Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes. Science 286:552-555.
50. Yang SW, Burgin AB, Jr, Huizenga BN, Robertson CA, Yao KC, Nash HA. 1996. A eukaryotic enzyme that can disjoin dead-end covalent complexes between DNA and type I topoisomerases. Proc. Natl. Acad. Sci. U. S. A. 93:11534-11539.