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BAP1 promotes the repair of UV-induced DNA damage via PARP1-mediated recruitment to damage sites and control of activity and stability

Cell Death & Differentiation volume 29, pages 2381–2398 (2022)Cite this article

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Abstract

BRCA1-associated protein-1 (BAP1) is a ubiquitin C-terminal hydrolase domain-containing deubiquitinase with tumor suppressor activity. The gene encoding BAP1 is mutated in various human cancers, with particularly high frequency in kidney and skin cancers, and BAP1 is involved in many cancer-related cellular functions, such as DNA repair and genome stability. Although BAP1 stimulates DNA double-strand break repair, whether it functions in nucleotide excision repair (NER) is unknown. Here, we show that BAP1 promotes the repair of ultraviolet (UV)-induced DNA damage via its deubiquitination activity in various cell types, including primary melanocytes. Poly(ADP-ribose) polymerase 1 (PARP1) interacts with and recruits BAP1 to damage sites, with BAP1 recruitment peaking after the DDB2 and XPC damage sensors. BAP1 recruitment also requires histone H2A monoubiquitinated at Lys119, which accumulates at damage sites. PARP1 transiently poly(ADP-ribosyl)ates (PARylates) BAP1 at multiple sites after UV damage and stimulates the deubiquitination activity of BAP1 both intrinsically and via PARylation. PARP1 also promotes BAP1 stability via crosstalk between PARylation and ubiquitination. Many PARylation sites in BAP1 are mutated in various human cancers, among which the glutamic acid (Glu) residue at position 31, with particularly frequent mutation in kidney cancer, plays a critical role in BAP1 stabilization and promotes UV-induced DNA damage repair. Glu31 also participates in reducing the viability of kidney cancer cells. This study therefore reveals that BAP1 functions in the NER pathway and that PARP1 plays a role as a novel factor that regulates BAP1 enzymatic activity, protein stability, and recruitment to damage sites. This activity of BAP1 in NER, along with its cancer cell viability-reducing activity, may account for its tumor suppressor function.

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Fig. 1: BAP1 is recruited to UV damage sites and promotes DNA repair.
Fig. 2: BAP1 interacts with PARP1 in response to UV damage.
Fig. 3: PARP1 PARylates BAP1 in response to UV damage.
Fig. 4: PARP1 recruits BAP1 to UV damage sites to promote DNA repair.
Fig. 5: PARP1 PARylates BAP1 at multiple sites in vitro.
Fig. 6: PARP1 regulates the catalytic activity of BAP1 intrinsically and via PARylation.
Fig. 7: The Glu31 PARylation site, frequently mutated in human cancers, promotes BAP1 stability and CPD repair.
Fig. 8: BAP1 Glu31 promotes CPD repair and reduces the viability of ccRCC cells.

Data availability

The detailed experimental procedures and the materials used in this study will be freely available upon request. Please contact jongkwon@ewha.ac.kr.

References

  1. Marteijn JA, Lans H, Vermeulen W, Hoeijmakers JH. Understanding nucleotide excision repair and its roles in cancer and ageing. Nat Rev Mol Cell Biol. 2014;15:465–81.

    Article  CAS  Google Scholar 

  2. Sugasawa K. Molecular mechanisms of DNA damage recognition for mammalian nucleotide excision repair. DNA Repair. 2016;44:110–7.

    Article  CAS  Google Scholar 

  3. Ray Chaudhuri A, Nussenzweig A. The multifaceted roles of PARP1 in DNA repair and chromatin remodelling. Nat Rev Mol Cell Biol. 2017;18:610–21.

    Article  CAS  Google Scholar 

  4. Kraus WL. PARPs and ADP-Ribosylation: 50 Years … and Counting. Mol Cell. 2015;58:902–10.

    Article  CAS  Google Scholar 

  5. Cohen MS, Chang P. Insights into the biogenesis, function, and regulation of ADP-ribosylation. Nat Chem Biol. 2018;14:236–43.

    Article  CAS  Google Scholar 

  6. Gupte R, Liu Z, Kraus WL. PARPs and ADP-ribosylation: recent advances linking molecular functions to biological outcomes. Genes & development. 2017;31:101–26.

    Article  CAS  Google Scholar 

  7. Alemasova EE, Lavrik OI. Poly(ADP-ribosyl)ation by PARP1: reaction mechanism and regulatory proteins. Nucleic Acids Res. 2019;47:3811–27.

    Article  CAS  Google Scholar 

  8. Robu M, Shah RG, Purohit NK, Zhou P, Naegeli H, Shah GM. Poly(ADP-ribose) polymerase 1 escorts XPC to UV-induced DNA lesions during nucleotide excision repair. Proc Natl Acad Sci USA. 2017;114:E6847–E6856.

    Article  CAS  Google Scholar 

  9. Robu M, Shah RG, Petitclerc N, Brind'Amour J, Kandan-Kulangara F, Shah GM. Role of poly(ADP-ribose) polymerase-1 in the removal of UV-induced DNA lesions by nucleotide excision repair. Proc Natl Acad Sci USA. 2013;110:1658–63.

    Article  CAS  Google Scholar 

  10. Pines A, Vrouwe MG, Marteijn JA, Typas D, Luijsterburg MS, Cansoy M, et al. PARP1 promotes nucleotide excision repair through DDB2 stabilization and recruitment of ALC1. J Cell Biol. 2012;199:235–49.

    Article  CAS  Google Scholar 

  11. King BS, Cooper KL, Liu KJ, Hudson LG. Poly(ADP-ribose) contributes to an association between poly(ADP-ribose) polymerase-1 and xeroderma pigmentosum complementation group A in nucleotide excision repair. J Biol Chem. 2012;287:39824–33.

    Article  CAS  Google Scholar 

  12. Jensen DE, Proctor M, Marquis ST, Gardner HP, Ha SI, Chodosh LA, et al. BAP1: a novel ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene. 1998;16:1097–112.

    Article  CAS  Google Scholar 

  13. Carbone M, Yang H, Pass HI, Krausz T, Testa JR, Gaudino G. BAP1 and cancer. Nat Rev Cancer. 2013;13:153–9.

    Article  CAS  Google Scholar 

  14. Masclef L, Ahmed O, Estavoyer B, Larrivee B, Labrecque N, Nijnik A, et al. Roles and mechanisms of BAP1 deubiquitinase in tumor suppression. Cell Death Differ. 2021;28:606–25.

    Article  CAS  Google Scholar 

  15. Szczepanski AP, Wang L. Emerging multifaceted roles of BAP1 complexes in biological processes. Cell Death Disco. 2021;7:20.

    Article  CAS  Google Scholar 

  16. Abdel-Rahman MH, Pilarski R, Cebulla CM, Massengill JB, Christopher BN, Boru G, et al. Germline BAP1 mutation predisposes to uveal melanoma, lung adenocarcinoma, meningioma, and other cancers. J Med Genet. 2011;48:856–9.

    Article  CAS  Google Scholar 

  17. Bott M, Brevet M, Taylor BS, Shimizu S, Ito T, Wang L, et al. The nuclear deubiquitinase BAP1 is commonly inactivated by somatic mutations and 3p21.1 losses in malignant pleural mesothelioma. Nat Genet. 2011;43:668–72.

    Article  CAS  Google Scholar 

  18. Guo G, Gui Y, Gao S, Tang A, Hu X, Huang Y, et al. Frequent mutations of genes encoding ubiquitin-mediated proteolysis pathway components in clear cell renal cell carcinoma. Nat Genet. 2012;44:17–19.

    Article  CAS  Google Scholar 

  19. Harbour JW, Onken MD, Roberson ED, Duan S, Cao L, Worley LA, et al. Frequent mutation of BAP1 in metastasizing uveal melanomas. Science. 2010;330:1410–3.

    Article  CAS  Google Scholar 

  20. Pena-Llopis S, Vega-Rubin-de-Celis S, Liao A, Leng N, Pavia-Jimenez A, Wang S, et al. BAP1 loss defines a new class of renal cell carcinoma. Nat Genet. 2012;44:751–9.

    Article  CAS  Google Scholar 

  21. Testa JR, Cheung M, Pei J, Below JE, Tan Y, Sementino E, et al. Germline BAP1 mutations predispose to malignant mesothelioma. Nat Genet. 2011;43:1022–5.

    Article  CAS  Google Scholar 

  22. Carbone M, Adusumilli PS, Alexander HR Jr, Baas P, Bardelli F, Bononi A, et al. Mesothelioma: Scientific clues for prevention, diagnosis, and therapy. CA Cancer J Clin. 2019;69:402–29.

    Article  Google Scholar 

  23. Napolitano A, Pellegrini L, Dey A, Larson D, Tanji M, Flores EG, et al. Minimal asbestos exposure in germline BAP1 heterozygous mice is associated with deregulated inflammatory response and increased risk of mesothelioma. Oncogene. 2016;35:1996–2002.

    Article  CAS  Google Scholar 

  24. Kadariya Y, Cheung M, Xu J, Pei J, Sementino E, Menges CW, et al. Bap1 Is a Bona Fide Tumor Suppressor: Genetic Evidence from Mouse Models Carrying Heterozygous Germline Bap1 Mutations. Cancer Res. 2016;76:2836–44.

    Article  CAS  Google Scholar 

  25. Xu J, Kadariya Y, Cheung M, Pei J, Talarchek J, Sementino E, et al. Germline mutation of Bap1 accelerates development of asbestos-induced malignant mesothelioma. Cancer Res. 2014;74:4388–97.

    Article  CAS  Google Scholar 

  26. Dey A, Seshasayee D, Noubade R, French DM, Liu J, Chaurushiya MS, et al. Loss of the tumor suppressor BAP1 causes myeloid transformation. Science. 2012;337:1541–6.

    Article  CAS  Google Scholar 

  27. Machida YJ, Machida Y, Vashisht AA, Wohlschlegel JA, Dutta A. The deubiquitinating enzyme BAP1 regulates cell growth via interaction with HCF-1. J Biol Chem. 2009;284:34179–88.

    Article  CAS  Google Scholar 

  28. Misaghi S, Ottosen S, Izrael-Tomasevic A, Arnott D, Lamkanfi M, Lee J, et al. Association of C-terminal ubiquitin hydrolase BRCA1-associated protein 1 with cell cycle regulator host cell factor 1. Mol Cell Biol. 2009;29:2181–92.

    Article  CAS  Google Scholar 

  29. Eletr ZM, Wilkinson KD. An emerging model for BAP1's role in regulating cell cycle progression. Cell Biochem Biophys. 2011;60:3–11.

    Article  CAS  Google Scholar 

  30. Affar EB, Carbone M. BAP1 regulates different mechanisms of cell death. Cell Death Dis. 2018;9:1151.

    Article  Google Scholar 

  31. Yu H, Pak H, Hammond-Martel I, Ghram M, Rodrigue A, Daou S, et al. Tumor suppressor and deubiquitinase BAP1 promotes DNA double-strand break repair. Proc Natl Acad Sci USA. 2014;111:285–90.

    Article  CAS  Google Scholar 

  32. Eletr ZM, Yin L, Wilkinson KD. BAP1 is phosphorylated at serine 592 in S-phase following DNA damage. FEBS Lett. 2013;587:3906–11.

    Article  CAS  Google Scholar 

  33. Klusmann I, Wohlberedt K, Magerhans A, Teloni F, Korbel JO, Altmeyer M, et al. Chromatin modifiers Mdm2 and RNF2 prevent RNA:DNA hybrids that impair DNA replication. Proc Natl Acad Sci USA. 2018;115:E11311–E11320.

    Article  CAS  Google Scholar 

  34. Lee HS, Lee SA, Hur SK, Seo JW, Kwon J. Stabilization and targeting of INO80 to replication forks by BAP1 during normal DNA synthesis. Nat Commun. 2014;5:5128.

    Article  CAS  Google Scholar 

  35. Lee HS, Seo HR, Lee SA, Choi S, Kang D, Kwon J. BAP1 promotes stalled fork restart and cell survival via INO80 in response to replication stress. Biochemical J. 2019;476:3053–66.

    Article  CAS  Google Scholar 

  36. Peng J, Ma J, Li W, Mo R, Zhang P, Gao K, et al. Stabilization of MCRS1 by BAP1 prevents chromosome instability in renal cell carcinoma. Cancer Lett. 2015;369:167–74.

    Article  CAS  Google Scholar 

  37. Ismail IH, Davidson R, Gagne JP, Xu ZZ, Poirier G, Hendzel MJ Germ-line Mutations in BAP1 Impair its Function in DNA Double-Strand break Repair. Cancer Res. 2014.

  38. Muster B, Rapp A, Cardoso MC. Systematic analysis of DNA damage induction and DNA repair pathway activation by continuous wave visible light laser micro-irradiation. AIMS Genet. 2017;4:47–68.

    Article  Google Scholar 

  39. Wakasugi M, Sasaki T, Matsumoto M, Nagaoka M, Inoue K, Inobe M, et al. Nucleotide excision repair-dependent DNA double-strand break formation and ATM signaling activation in mammalian quiescent cells. J Biol Chem. 2014;289:28730–7.

    Article  CAS  Google Scholar 

  40. Ray A, Milum K, Battu A, Wani G, Wani AA. NER initiation factors, DDB2 and XPC, regulate UV radiation response by recruiting ATR and ATM kinases to DNA damage sites. DNA Repair. 2013;12:273–83.

    Article  CAS  Google Scholar 

  41. Zhang Y, Wang J, Ding M, Yu Y. Site-specific characterization of the Asp- and Glu-ADP-ribosylated proteome. Nat Methods. 2013;10:981–4.

    Article  CAS  Google Scholar 

  42. Gibson BA, Kraus WL. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol. 2012;13:411–24.

    Article  CAS  Google Scholar 

  43. Bergink S, Salomons FA, Hoogstraten D, Groothuis TA, de Waard H, Wu J, et al. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev. 2006;20:1343–52.

    Article  CAS  Google Scholar 

  44. Kapetanaki MG, Guerrero-Santoro J, Bisi DC, Hsieh CL, Rapic-Otrin V, Levine AS. The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc Natl Acad Sci USA. 2006;103:2588–93.

    Article  CAS  Google Scholar 

  45. Zhu Q, Wani G, Arab HH, El-Mahdy MA, Ray A, Wani AA. Chromatin restoration following nucleotide excision repair involves the incorporation of ubiquitinated H2A at damaged genomic sites. DNA Repair. 2009;8:262–73.

    Article  CAS  Google Scholar 

  46. Chitale S, Richly HDICER. and ZRF1 contribute to chromatin decondensation during nucleotide excision repair. Nucleic Acids Res. 2017;45:5901–12.

    Article  CAS  Google Scholar 

  47. Marteijn JA, Bekker-Jensen S, Mailand N, Lans H, Schwertman P, Gourdin AM, et al. Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response. Cell Biol. 2009;186:835–47.

    Article  CAS  Google Scholar 

  48. Sarkar S, Kiely R, McHugh PJ. The Ino80 chromatin-remodeling complex restores chromatin structure during UV DNA damage repair. J Cell Biol. 2010;191:1061–8.

    Article  CAS  Google Scholar 

  49. Jiang Y, Wang X, Bao S, Guo R, Johnson DG, Shen X, et al. INO80 chromatin remodeling complex promotes the removal of UV lesions by the nucleotide excision repair pathway. Proc Natl Acad Sci USA. 2010;107:17274–9.

    Article  CAS  Google Scholar 

  50. Rathkey D, Khanal M, Murai J, Zhang J, Sengupta M, Jiang Q, et al. Sensitivity of Mesothelioma Cells to PARP Inhibitors Is Not Dependent on BAP1 but Is Enhanced by Temozolomide in Cells With High-Schlafen 11 and Low-O6-methylguanine-DNA Methyltransferase Expression. J Thorac Oncol. 2020;15:843–59.

    Article  CAS  Google Scholar 

  51. Carbone M, Pass HI, Ak G, Alexander HR Jr, Baas P, Baumann F, et al. Medical and surgical care of mesothelioma patients and their relatives carrying germline BAP1 mutations. J Thorac Oncol. 2022;S1556-0864:00192–7.

    Google Scholar 

  52. Ghafoor A, Mian I, Wagner C, Mallory Y, Agra MG, Morrow B, et al. Phase 2 Study of Olaparib in Malignant Mesothelioma and Correlation of Efficacy With Germline or Somatic Mutations in BAP1. Gene. JTO Clin Res Rep. 2021;2:100231.

    Google Scholar 

  53. Bononi A, Giorgi C, Patergnani S, Larson D, Verbruggen K, Tanji M, et al. BAP1 regulates IP3R3-mediated Ca(2+) flux to mitochondria suppressing cell transformation. Nature. 2017;546:549–53.

    Article  CAS  Google Scholar 

  54. Sime W, Niu Q, Abassi Y, Masoumi KC, Zarrizi R, Kohler JB, et al. BAP1 induces cell death via interaction with 14-3-3 in neuroblastoma. Cell Death Dis. 2018;9:458.

    Article  Google Scholar 

  55. He M, Chaurushiya MS, Webster JD, Kummerfeld S, Reja R, Chaudhuri S, et al. Intrinsic apoptosis shapes the tumor spectrum linked to inactivation of the deubiquitinase BAP1. Science. 2019;364:283–5.

    Article  CAS  Google Scholar 

  56. Zhang Y, Shi J, Liu X, Feng L, Gong Z, Koppula P, et al. BAP1 links metabolic regulation of ferroptosis to tumour suppression. Nat Cell Biol. 2018;20:1181–92.

    Article  CAS  Google Scholar 

  57. Lee JW, Kim JE, Park EJ, Kim JH, Lee CH, Lee SR, et al. Two conserved cysteine residues are critical for the enzymic function of the human platelet-derived growth factor receptor-beta: evidence for different roles of Cys-822 and Cys-940 in the kinase activity. Biochem J. 2004;382:631–9.

    Article  CAS  Google Scholar 

  58. Lee D, Lee DY, Hwang YS, Seo HR, Lee SA, Kwon J. The Bromodomain Inhibitor PFI-3 Sensitizes Cancer Cells to DNA Damage by Targeting SWI/SNF. Mol Cancer Res: MCR. 2021;19:900–12.

    Article  Google Scholar 

  59. Robu M, Shah RG, Shah GM. Methods to Study Intracellular Movement and Localization of the Nucleotide Excision Repair Proteins at the DNA Lesions in Mammalian Cells. Front Cell Dev Biol. 2020;8:590242.

    Article  Google Scholar 

  60. Park SG, Lee D, Seo HR, Lee SA, Kwon J. Cytotoxic activity of bromodomain inhibitor NVS-CECR2-1 on human cancer cells. Sci Rep. 2020;10:16330.

    Article  CAS  Google Scholar 

  61. Sahtoe DD, van Dijk WJ, Ekkebus R, Ovaa H, Sixma TK. BAP1/ASXL1 recruitment and activation for H2A deubiquitination. Nat Commun. 2016;7:10292.

    Article  CAS  Google Scholar 

  62. Mashtalir N, Daou S, Barbour H, Sen NN, Gagnon J, Hammond-Martel I, et al. Autodeubiquitination protects the tumor suppressor BAP1 from cytoplasmic sequestration mediated by the atypical ubiquitin ligase UBE2O. Mol Cell. 2014;54:392–406.

    Article  CAS  Google Scholar 

  63. Seo HR, Jeong D, Lee S, Lee HS, Lee SA, Kang SW, et al. CHIP and BAP1 Act in Concert to Regulate INO80 Ubiquitination and Stability for DNA Replication. Molecules Cells. 2021;44:101–15.

    Article  CAS  Google Scholar 

  64. Soo Lee N, Jin Chung H, Kim HJ, Yun Lee S, Ji JH, Seo Y, et al. TRAIP/RNF206 is required for recruitment of RAP80 to sites of DNA damage. Nat Commun. 2016;7:10463.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Mi Young Kim and William Kraus for providing the pQCXIH-PARP1-His6/FLAG vector. Funding: This work was supported by grants 2021R1A2C1008613, 2019R1A5A6099645 and 2017M3A9F9030559 from the National Research Foundation of Korea.

Funding

This work was supported by grants 2021R1A2C1008613, 2019R1A5A6099645 and 2017M3A9F9030559 from the National Research Foundation of Korea.

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Author notes

  1. Shin-Ai Lee

    Present address: Laboratory of Genitourinary Cancer Pathogenesis, Center for Cancer Research, National Cancer Institute, Building 37, Room 1068, Bethesda, MD, 20892-4263, USA

  2. These authors contributed equally: Shin-Ai Lee, Daye Lee, Minhwa Kang, Sora Kim.

Authors and Affiliations

  1. Department of Life Science, The Research Center for Cellular Homeostasis, Ewha Womans University, 52 Ewhayeodae-gil, Seodaemun-gu, Seoul, 03760, Korea

    Shin-Ai Lee, Daye Lee, Minhwa Kang, Sora Kim, Su-Jung Kwon, Han-Sae Lee, Hye-Ran Seo & Jongbum Kwon

  2. Center for Theragnosis, Korea Institute of Science and Technology, Seoul, 02792, Korea

    Prashant Kaushal & Cheolju Lee

  3. Division of Bio-Medical Science & Technology, KIST School, Korea University of Science and Technology, Seoul, 02792, Korea

    Prashant Kaushal

  4. Department of Biological Sciences, Sungkyunkwan University, Suwon, 16419, Korea

    Nam Soo Lee

  5. School of Life Sciences, Ulsan National Institute of Science and Technology, Ulsan, 44919, Korea

    Hongtae Kim

  6. KHU-KIST Department of Converging Science and Technology, Kyung Hee University, 26 Kyunghee-daero, Dongdaemun-gu, Seoul, 02447, Korea

    Cheolju Lee

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Contributions

SAL initiated the study and generated most of the key initial data. DL produced the data for the repair activity of BAP1 and the related functions of PARP1. MK generated the data for the PARP1 effects on BAP1 activity, and SK for the in vivo BAP1 PARylation and the functional analysis of the BAP1 PARylation sites. SJK was responsible for the identification of PARP1 as a BAP1 binding partner. HRS obtained the results for the PARPi effects on BAP1 stability. PK and CL identified the BAP1 PARylation sites by LC-MS/MS. NSL and HK generated the laser microirradiation data. HSL provided important technical assistance and data interpretation. All authors contributed to data analysis and interpretation, and manuscript preparation. SAL and JK wrote the manuscript. JK conceived and supervised the entire project.

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Correspondence to Jongbum Kwon.

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Lee, SA., Lee, D., Kang, M. et al. BAP1 promotes the repair of UV-induced DNA damage via PARP1-mediated recruitment to damage sites and control of activity and stability. Cell Death Differ 29, 2381–2398 (2022). https://doi.org/10.1038/s41418-022-01024-w

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