TRAIP regulates Histone H2B monoubiquitination in DNA damage response pathways

  • Authors:
    • Ye Gi Han
    • Miyong Yun
    • Minji Choi
    • Seok‑Geun Lee
    • Hongtae Kim
  • View Affiliations

  • Published online on: April 2, 2019     https://doi.org/10.3892/or.2019.7092
  • Pages: 3305-3312
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )


Abstract

Histone H2B monoubiquitination has been shown to play critical roles in diverse cellular processes including DNA damage response. Although recent data indicate that H2B monoubiquitination is strongly connected with tumor progression and regulation, the implications of this modification in lung adenocarcinoma are relatively unknown. In the present study, we demonstrated the clinical implication of H2B monoubiquitination and the potential role of tumor necrosis factor receptor‑associated factor‑interacting protein (TRAIP) in regulating its modification in lung adenocarcinoma. Immunohistochemical analysis showed that H2B monoubiquitination was significantly downregulated in 68 human lung adenocarcinoma patient samples compared to their normal adjacent tissues. Depletion of TRAIP by specific siRNA treatment markedly decreased ionizing radiation (IR)‑induced H2B monoubiquitination. In addition, deletion mutants without RING domain or C‑terminus of TRAIP diminished the ability to induce H2B monoubiquitination at lysine 120. Notably, the nuclear expression of TRAIP was positively related with H2B monoubiquitination levels in patients with lung adenocarcinoma. Furthermore, statistical analysis indicated that low levels of both TRAIP and H2B monoubiquitination, not each alone, in patients with lung adenocarcinoma were strongly correlated with poor survival. Taken together, these results suggest that TRAIP is a novel regulator of H2B monoubiquitination in DNA damage response and cancer development in lung adenocarcinoma.

References

1 

Durocher D and Jackson SP: DNA-PK, ATM and ATR as sensors of DNA damage: Variations on a theme? Curr Opin Cell Biol. 13:225–231. 2001. View Article : Google Scholar : PubMed/NCBI

2 

Kerzendorfer C and O'Driscoll M: Human DNA damage response and repair deficiency syndromes: Linking genomic instability and cell cycle checkpoint proficiency. DNA Rep. 8:1139–1152. 2009. View Article : Google Scholar

3 

Uckelmann M and Sixma TK: Histone ubiquitination in the DNA damage response. DNA Repair. 56:92–101. 2017. View Article : Google Scholar : PubMed/NCBI

4 

Dantuma NP and van Attikum H: Spatiotemporal regulation of posttranslational modifications in the DNA damage response. EMBO J. 35:6–23. 2016. View Article : Google Scholar : PubMed/NCBI

5 

Fuchs G, Shema E, Vesterman R, Kotler E, Wolchinsky Z, Wilder S, Golomb L, Pribluda A, Zhang F, Haj-Yahya M, et al: RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation. Mol Cell. 46:662–673. 2012. View Article : Google Scholar : PubMed/NCBI

6 

Minsky N, Shema E, Field Y, Schuster M, Segal E and Oren M: Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat Cell Biol. 10:483–488. 2008. View Article : Google Scholar : PubMed/NCBI

7 

Zhu B, Zheng Y, Pham AD, Mandal SS, Erdjument-Bromage H, Tempst P and Reinberg D: Monoubiquitination of human Histone H2B: The factors involved and their roles in HOX gene regulation. Mol Cell. 20:601–611. 2005. View Article : Google Scholar : PubMed/NCBI

8 

Thorne AW, Sautiere P, Briand G and Crane-Robinson C: The structure of ubiquitinated Histone H2B. EMBO J. 6:1005–1010. 1987. View Article : Google Scholar : PubMed/NCBI

9 

Weake VM and Workman JL: Histone ubiquitination: Triggering gene activity. Mol Cell. 29:653–663. 2008. View Article : Google Scholar : PubMed/NCBI

10 

Shanbhag NM, Rafalska-Metcalf IU, Balane-Bolivar C, Janicki SM and Greenberg RA: ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell. 141:970–981. 2010. View Article : Google Scholar : PubMed/NCBI

11 

Xu Z, Song Z, Li G, Tu H, Liu W, Liu Y, Wang P, Wang Y, Cui X, Liu C, et al: H2B ubiquitination regulates meiotic recombination by promoting chromatin relaxation. Nucleic Acids Res. 44:9681–9697. 2016.PubMed/NCBI

12 

Pavri R, Zhu B, Li G, Trojer P, Mandal S, Shilatifard A and Reinberg D: Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell. 125:703–717. 2006. View Article : Google Scholar : PubMed/NCBI

13 

Zhang XY, Varthi M, Sykes SM, Phillips C, Warzecha C, Zhu W, Wyce A, Thorne AW, Berger SL and McMahon SB: The putative cancer stem cell marker USP22 is a subunit of the human SAGA complex required for activated transcription and cell-cycle progression. Mol Cell. 29:102–111. 2008. View Article : Google Scholar : PubMed/NCBI

14 

Shema E, Tirosh I, Aylon Y, Huang J, Ye C, Moskovits N, Raver-Shapira N, Minsky N, Pirngruber J, Tarcic G, et al: The Histone H2B-specific ubiquitin ligase RNF20/hBRE1 acts as a putative tumor suppressor through selective regulation of gene expression. Genes Dev. 22:2664–2676. 2008. View Article : Google Scholar : PubMed/NCBI

15 

Moyal L, Lerenthal Y, Gana-Weisz M, Mass G, So S, Wang SY, Eppink B, Chung YM, Shalev G, Shema E, et al: Requirement of ATM-dependent monoubiquitylation of Histone H2B for timely repair of DNA double-strand breaks. Mol Cell. 41:529–542. 2011. View Article : Google Scholar : PubMed/NCBI

16 

Lee SY and Choi Y: TRAF-interacting protein (TRIP): A novel component of the tumor necrosis factor receptor (TNFR)-and CD30-TRAF signaling complexes that inhibits TRAF2-mediated NF-kappaB activation. J Exp Med. 185:1275–1286. 1997. View Article : Google Scholar : PubMed/NCBI

17 

Rothe M, Pan MG, Henzel WJ, Ayres TM and Goeddel DV: The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell. 83:1243–1252. 1995. View Article : Google Scholar : PubMed/NCBI

18 

Besse A, Campos AD, Webster WK and Darnay BG: TRAF-interacting protein (TRIP) is a RING-dependent ubiquitin ligase. Biochem Biophys Res Commun. 359:660–664. 2007. View Article : Google Scholar : PubMed/NCBI

19 

Regamey A, Hohl D, Liu JW, Roger T, Kogerman P, Toftgard R and Huber M: The tumor suppressor CYLD interacts with TRIP and regulates negatively nuclear factor kappaB activation by tumor necrosis factor. J Exp Med. 198:1959–1964. 2003. View Article : Google Scholar : PubMed/NCBI

20 

Zhou Q and Geahlen R: The protein-tyrosine kinase Syk interacts with TRAF-interacting protein TRIP in breast epithelial cells. Oncogene. 28:1348–1356. 2009. View Article : Google Scholar : PubMed/NCBI

21 

Deshaies RJ and Joazeiro CA: RING domain E3 ubiquitin ligases. Annu Rev Biochem. 78:399–434. 2009. View Article : Google Scholar : PubMed/NCBI

22 

Chapard C, Meraldi P, Gleich T, Bachmann D, Hohl D and Huber M: TRAIP is a regulator of the spindle assembly checkpoint. J Cell Sci. 127:5149–5156. 2014. View Article : Google Scholar : PubMed/NCBI

23 

Harley ME, Murina O, Leitch A, Higgs MR, Bicknell LS, Yigit G, Blackford AN, Zlatanou A, Mackenzie KJ, Reddy K, et al: TRAIP promotes DNA damage response during genome replication and is mutated in primordial dwarfism. Nat Genet. 48:36–43. 2016. View Article : Google Scholar : PubMed/NCBI

24 

Feng W, Guo Y, Huang J, Deng Y, Zang J and Huen MS: TRAIP regulates replication fork recovery and progression via PCNA. Cell Discov. 2:160162016. View Article : Google Scholar : PubMed/NCBI

25 

Soo Lee N, Jin Chung H, Kim HJ, Yun Lee S, Ji JH, Seo Y, Hun Han S, Choi M, Yun M, Lee SG, et al: TRAIP/RNF206 is required for recruitment of RAP80 to sites of DNA damage. Nat Commun. 7:104632016. View Article : Google Scholar : PubMed/NCBI

26 

Hoffmann S, Smedegaard S, Nakamura K, Mortuza GB, Räschle M, Ibañez de Opakua A, Oka Y, Feng Y, Blanco FJ, Mann M, et al: TRAIP is a PCNA-binding ubiquitin ligase that protects genome stability after replication stress. J Cell Biol. 212:63–75. 2016. View Article : Google Scholar : PubMed/NCBI

27 

Kim H, Huang J and Chen J: CCDC98 is a BRCA1-BRCT domain-binding protein involved in the DNA damage response. Nat Struct Mol Biol. 14:710–715. 2007. View Article : Google Scholar : PubMed/NCBI

28 

Kim H, Chen J and Yu X: Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science. 316:1202–1205. 2007. View Article : Google Scholar : PubMed/NCBI

29 

Lorick KL, Jensen JP, Fang S, Ong AM, Hatakeyama S and Weissman AM: RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci USA. 96:11364–11369. 1999. View Article : Google Scholar : PubMed/NCBI

30 

Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin. 61:69–90. 2011. View Article : Google Scholar : PubMed/NCBI

31 

Dela Cruz CS, Tanoue LT and Matthay RA: Lung cancer: Epidemiology, etiology, and prevention. Clin Chest Med. 32:605–644. 2011. View Article : Google Scholar : PubMed/NCBI

32 

Molina JR, Yang P, Cassivi SD, Schild SE and Adjei AA: Non-small cell lung cancer: Epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc. 83:584–594. 2008. View Article : Google Scholar : PubMed/NCBI

33 

Jung Y and Lippard SJ: Direct cellular responses to platinum-induced DNA damage. Chem Rev. 107:1387–1407. 2007. View Article : Google Scholar : PubMed/NCBI

34 

Pearl LH, Schierz AC, Ward SE, Al-Lazikani B and Pearl FM: Therapeutic opportunities within the DNA damage response. Nat Rev Cancer. 15:166–180. 2015. View Article : Google Scholar : PubMed/NCBI

35 

Jackson SP and Bartek J: The DNA-damage response in human biology and disease. Nature. 461:1071–1078. 2009. View Article : Google Scholar : PubMed/NCBI

36 

European Medicines Agency: Lynparza recommended for approval in ovarian cancer. simplehttps://www.ema.europa.eu/en/news/lynparza-recommended-approval-ovarian-cancer

37 

Chen S, Jing Y, Kang X, Yang L, Wang DL, Zhang W, Zhang L, Chen P, Chang JF, Yang XM, et al: Histone H2B monoubiquitination is a critical epigenetic switch for the regulation of autophagy. Nucleic Acids Res. 45:1144–1158. 2017.PubMed/NCBI

38 

Jackson SP and Durocher D: Regulation of DNA damage responses by ubiquitin and SUMO. Mol Cell. 49:795–807. 2013. View Article : Google Scholar : PubMed/NCBI

39 

Schwertman P, Bekker-Jensen S and Mailand N: Regulation of DNA double-strand break repair by ubiquitin and ubiquitin-like modifiers. Nat Rev Mol Cell Biol. 17:379–394. 2016. View Article : Google Scholar : PubMed/NCBI

40 

Mattiroli F, Vissers JH, van Dijk WJ, Ikpa P, Citterio E, Vermeulen W, Marteijn JA and Sixma TK: RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell. 150:1182–1195. 2012. View Article : Google Scholar : PubMed/NCBI

41 

Kalb R, Mallery DL, Larkin C, Huang JT and Hiom K: BRCA1 is a histone-H2A-specific ubiquitin ligase. Cell Rep. 8:999–1005. 2014. View Article : Google Scholar : PubMed/NCBI

42 

Wood A, Krogan NJ, Dover J, Schneider J, Heidt J, Boateng MA, Dean K, Golshani A, Zhang Y, Greenblatt JF, et al: Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol Cell. 11:267–274. 2003. View Article : Google Scholar : PubMed/NCBI

43 

Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS and Zhang Y: Role of histone H2A ubiquitination in polycomb silencing. Nature. 431:873–878. 2004. View Article : Google Scholar : PubMed/NCBI

44 

Wallace HA, Merkle JA, Yu MC, Berg TG, Lee E, Bosco G and Lee LA: TRIP/NOPO E3 ubiquitin ligase promotes ubiquitylation of DNA polymerase η. Development. 141:1332–1341. 2014. View Article : Google Scholar : PubMed/NCBI

Related Articles

Journal Cover

June 2019
Volume 41 Issue 6

Print ISSN: 1021-335X
Online ISSN:1791-2431

Sign up for eToc alerts

Recommend to Library

Copy and paste a formatted citation
APA
Han, Y.G., Yun, M., Choi, M., Lee, S., & Kim, H. (2019). TRAIP regulates Histone H2B monoubiquitination in DNA damage response pathways. Oncology Reports, 41, 3305-3312. https://doi.org/10.3892/or.2019.7092
MLA
Han, Y. G., Yun, M., Choi, M., Lee, S., Kim, H."TRAIP regulates Histone H2B monoubiquitination in DNA damage response pathways". Oncology Reports 41.6 (2019): 3305-3312.
Chicago
Han, Y. G., Yun, M., Choi, M., Lee, S., Kim, H."TRAIP regulates Histone H2B monoubiquitination in DNA damage response pathways". Oncology Reports 41, no. 6 (2019): 3305-3312. https://doi.org/10.3892/or.2019.7092