UCHL3 Regulates Topoisomerase-Induced Chromosomal Break Repair by Controlling TDP1 Proteostasis

Cell Reports

Volumn 23, Issue 11, 2018, Pages 3352-3365

  Liao, Chunyan ^a   Beveridge, Ryan ^a   Hudson, Jessica J R ^a,b   Parker, Jacob D ^a   Chiang, Shih Chieh ^a   Ray, Swagat ^a   Ashour, Mohamed E ^c   Sudbery, Ian ^a   Dickman, Mark J ^a   El Khamisy, Sherif F ^a,c  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c ZEWAIL CITY OF SCIENCE AND TECHNOLOGY   (Egypt)

Author keywords

aging; cancer; heart failure; myocardial infarction; neurodegeneration; rhabdosarcoma; SCAN1; TDP; topoisomerase; UCHL3

Indexed keywords

DNA TOPOISOMERASE; MESSENGER RNA; PHOSPHODIESTERASE I; REGULATOR PROTEIN; TYROSYL DNA PHOSPHODIESTERASE 1; UBIQUITIN CARBOXY TERMINAL HYDROLASE L3; UBIQUITIN THIOLESTERASE; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG; CANT1 PROTEIN, HUMAN; CYSTEINE PROTEINASE; NUCLEOTIDASE; PHOSPHODIESTERASE; SMALL INTERFERING RNA; TDP1 PROTEIN, HUMAN; UBIQUITIN; UCHL3 PROTEIN, HUMAN;

ARTICLE; CHROMOSOME BREAKAGE; CONTROLLED STUDY; DNA REPAIR; DOWN REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MRNA EXPRESSION LEVEL; NUCLEOTIDE SEQUENCE; PROTEIN DEPLETION; PROTEIN HOMEOSTASIS; RHABDOMYOSARCOMA CELL; TURNOVER TIME; UBIQUITINATION; UPREGULATION; CHEMISTRY; GENETICS; HEK293 CELL LINE; METABOLISM; RNA INTERFERENCE; TUMOR CELL LINE;

CELL LINE, TUMOR; CHROMOSOME BREAKAGE; CYSTEINE ENDOPEPTIDASES; DNA REPAIR; DNA TOPOISOMERASES, TYPE I; DOWN-REGULATION; HEK293 CELLS; HUMANS; NUCLEOTIDASES; PHOSPHORIC DIESTER HYDROLASES; PROTEOSTASIS; RNA INTERFERENCE; RNA, SMALL INTERFERING; UBIQUITIN; UBIQUITINATION; UP-REGULATION;

EID: 85048266736     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2018.05.033     Document Type: Article

References (71)

1. Alagoz, M., Chiang, S.-C., Sharma, A., El-Khamisy, S.F., ATM deficiency results in accumulation of DNA-topoisomerase I covalent intermediates in neural cells. PLoS ONE, 8, 2013, e58239.
2. Alagoz, M., Wells, O.S., El-Khamisy, S.F., TDP1 deficiency sensitizes human cells to base damage via distinct topoisomerase I and PARP mechanisms with potential applications for cancer therapy. Nucleic Acids Res. 42 (2014), 3089–3103.
3. Amm, I., Sommer, T., Wolf, D.H., Protein quality control and elimination of protein waste: the role of the ubiquitin-proteasome system. Biochim. Biophys. Acta 1843 (2014), 182–196.
4. Artavanis-Tsakonas, K., Weihofen, W.A., Antos, J.M., Coleman, B.I., Comeaux, C.A., Duraisingh, M.T., Gaudet, R., Ploegh, H.L., Characterization and structural studies of the Plasmodium falciparum ubiquitin and Nedd8 hydrolase UCHL3. J. Biol. Chem. 285 (2010), 6857–6866.
5. Ashour, M.E., Atteya, R., El-Khamisy, S.F., Topoisomerase-mediated chromosomal break repair: an emerging player in many games. Nat. Rev. Cancer 15 (2015), 137–151.
6. Balch, W.E., Morimoto, R.I., Dillin, A., Kelly, J.W., Adapting proteostasis for disease intervention. Science 319 (2008), 916–919.
7. Barthelmes, H.U., Habermeyer, M., Christensen, M.O., Mielke, C., Interthal, H., Pouliot, J.J., Boege, F., Marko, D., TDP1 overexpression in human cells counteracts DNA damage mediated by topoisomerases I and II. J. Biol. Chem. 279 (2004), 55618–55625.
8. Breslin, C., Clements, P.M., El-Khamisy, S.F., Petermann, E., Iles, N., Caldecott, K.W., Measurement of chromosomal DNA single-strand breaks and replication fork progression rates. Methods Enzymol. 409 (2006), 410–425.
9. Champoux, J.J., Dulbecco, R., An activity from mammalian cells that untwists superhelical DNA–a possible swivel for DNA replication (polyoma-ethidium bromide-mouse-embryo cells-dye binding assay). Proc. Natl. Acad. Sci. USA 69 (1972), 143–146.
10. Chen, J., Chen, Z.J., Regulation of NF-κB by ubiquitination. Curr. Opin. Immunol. 25 (2013), 4–12.
11. Chiang, S.-C., Meagher, M., Kassouf, N., Hafezparast, M., McKinnon, P.J., Haywood, R., El-Khamisy, S.F., Mitochondrial protein-linked DNA breaks perturb mitochondrial gene transcription and trigger free radical-induced DNA damage. Sci. Adv., 3, 2017, e1602506.
12. Cortes Ledesma, F., El Khamisy, S.F., Zuma, M.C., Osborn, K., Caldecott, K.W., A human 5′-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature 461 (2009), 674–678.
13. Cuya, S.M., Comeaux, E.Q., Wanzeck, K., Yoon, K.J., van Waardenburg, R.C.A.M., Dysregulated human Tyrosyl-DNA phosphodiesterase I acts as cellular toxin. Oncotarget 7 (2016), 86660–86674.
14. Das, B.B., Antony, S., Gupta, S., Dexheimer, T.S., Redon, C.E., Garfield, S., Shiloh, Y., Pommier, Y., Optimal function of the DNA repair enzyme TDP1 requires its phosphorylation by ATM and/or DNA-PK. EMBO J. 28 (2009), 3667–3680.
15. Das, B.B., Huang, S.-Y.N., Murai, J., Rehman, I., Amé J.-C., Sengupta, S., Das, S.K., Majumdar, P., Zhang, H., Biard, D., et al. PARP1-TDP1 coupling for the repair of topoisomerase I-induced DNA damage. Nucleic Acids Res. 42 (2014), 4435–4449.
16. Do, P.M., Varanasi, L., Fan, S., Li, C., Kubacka, I., Newman, V., Chauhan, K., Daniels, S.R., Boccetta, M., Garrett, M.R., et al. Mutant p53 cooperates with ETS2 to promote etoposide resistance. Genes Dev. 26 (2012), 830–845.
17. Doil, C., Mailand, N., Bekker-Jensen, S., Menard, P., Larsen, D.H., Pepperkok, R., Ellenberg, J., Panier, S., Durocher, D., Bartek, J., et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136 (2009), 435–446.
18. Duffy, S., Fam, H.K., Wang, Y.K., Styles, E.B., Kim, J.-H., Ang, J.S., Singh, T., Larionov, V., Shah, S.P., Andrews, B., et al. Overexpression screens identify conserved dosage chromosome instability genes in yeast and human cancer. Proc. Natl. Acad. Sci. USA 113 (2016), 9967–9976.
19. El-Khamisy, S.F., To live or to die: a matter of processing damaged DNA termini in neurons. EMBO Mol. Med. 3 (2011), 78–88.
20. El-Khamisy, S.F., Saifi, G.M., Weinfeld, M., Johansson, F., Helleday, T., Lupski, J.R., Caldecott, K.W., Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1. Nature 434 (2005), 108–113.
21. Elserafy, M., El-Khamisy, S.F., Choose your yeast strain carefully: the RAD5 gene matters. Nat. Rev. Mol. Cell Biol., 2018, 10.1038/s41580-018-0005-2 Published online April 3, 2018.
22. Francisco, T., Rodrigues, T.A., Pinto, M.P., Carvalho, A.F., Azevedo, J.E., Grou, C.P., Ubiquitin in the peroxisomal protein import pathway. Biochimie 98 (2014), 29–35.
23. Frickel, E.-M., Quesada, V., Muething, L., Gubbels, M.-J., Spooner, E., Ploegh, H., Artavanis-Tsakonas, K., Apicomplexan UCHL3 retains dual specificity for ubiquitin and Nedd8 throughout evolution. Cell. Microbiol. 9 (2007), 1601–1610.
24. Garinis, G.A., Uittenboogaard, L.M., Stachelscheid, H., Fousteri, M., van Ijcken, W., Breit, T.M., van Steeg, H., Mullenders, L.H.F., van der Horst, G.T.J., Brüning, J.C., et al. Persistent transcription-blocking DNA lesions trigger somatic growth attenuation associated with longevity. Nat. Cell Biol. 11 (2009), 604–615.
25. Gómez-Herreros, F., Schuurs-Hoeijmakers, J.H.M., McCormack, M., Greally, M.T., Rulten, S., Romero-Granados, R., Counihan, T.J., Chaila, E., Conroy, J., Ennis, S., et al. TDP2 protects transcription from abortive topoisomerase activity and is required for normal neural function. Nat. Genet. 46 (2014), 516–521.
26. Hudson, J.J.R., Chiang, S.-C., Wells, O.S., Rookyard, C., El-Khamisy, S.F., SUMO modification of the neuroprotective protein TDP1 facilitates chromosomal single-strand break repair. Nat. Commun., 3, 2012 733–13.
27. Huen, M.S.Y., Grant, R., Manke, I., Minn, K., Yu, X., Yaffe, M.B., Chen, J., RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131 (2007), 901–914.
28. Interthal, H., Chen, H.J., Kehl-Fie, T.E., Zotzmann, J., Leppard, J.B., Champoux, J.J., SCAN1 mutant Tdp1 accumulates the enzyme–DNA intermediate and causes camptothecin hypersensitivity. EMBO J. 24 (2005), 2224–2233.
29. Jackson, S.P., Durocher, D., Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 49 (2013), 795–807.
30. Jiang, D., Zhang, Y., Hart, R.P., Chen, J., Herrup, K., Li, J., Alteration in 5-hydroxymethylcytosine-mediated epigenetic regulation leads to Purkinje cell vulnerability in ATM deficiency. Brain 138 (2015), 3520–3536.
31. Kannouche, P.L., Lehmann, A.R., Ubiquitination of PCNA and the polymerase switch in human cells. Cell Cycle 3 (2004), 1011–1013.
32. Kannouche, P.L., Wing, J., Lehmann, A.R., Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14 (2004), 491–500.
33. Katyal, S., el-Khamisy, S.F., Russell, H.R., Li, Y., Ju, L., Caldecott, K.W., McKinnon, P.J., TDP1 facilitates chromosomal single-strand break repair in neurons and is neuroprotective in vivo. EMBO J. 26 (2007), 4720–4731.
34. Katyal, S., Lee, Y., Nitiss, K.C., Downing, S.M., Li, Y., Shimada, M., Zhao, J., Russell, H.R., Petrini, J.H.J., Nitiss, J.L., McKinnon, P.J., Aberrant topoisomerase-1 DNA lesions are pathogenic in neurodegenerative genome instability syndromes. Nat. Neurosci. 17 (2014), 813–821.
35. Kerzendorfer, C., Whibley, A., Carpenter, G., Outwin, E., Chiang, S.-C., Turner, G., Schwartz, C., El-Khamisy, S., Raymond, F.L., O'Driscoll, M., Mutations in Cullin 4B result in a human syndrome associated with increased camptothecin-induced topoisomerase I-dependent DNA breaks. Hum. Mol. Genet. 19 (2010), 1324–1334.
36. Kiianitsa, K., Maizels, N., A rapid and sensitive assay for DNA-protein covalent complexes in living cells. Nucleic Acids Res., 41, 2013, e104.
37. Kim, J.Y., Lee, J.-M., Cho, J.-Y., Ubiquitin C-terminal hydrolase-L3 regulates Smad1 ubiquitination and osteoblast differentiation. FEBS Lett. 585 (2011), 1121–1126.
38. Komander, D., Clague, M.J., Urbé S., Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10 (2009), 550–563.
39. Liu, C., Zhou, S., Begum, S., Sidransky, D., Westra, W.H., Brock, M., Califano, J.A., Increased expression and activity of repair genes TDP1 and XPF in non-small cell lung cancer. Lung Cancer 55 (2007), 303–311.
40. Luo, K., Li, L., Li, Y., Wu, C., Yin, Y., Chen, Y., Deng, M., Nowsheen, S., Yuan, J., Lou, Z., A phosphorylation-deubiquitination cascade regulates the BRCA2-RAD51 axis in homologous recombination. Genes Dev. 30 (2016), 2581–2595.
41. Mailand, N., Bekker-Jensen, S., Faustrup, H., Melander, F., Bartek, J., Lukas, C., Lukas, J., RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131 (2007), 887–900.
42. Mattiroli, F., Vissers, J.H.A., van Dijk, W.J., Ikpa, P., Citterio, E., Vermeulen, W., Marteijn, J.A., Sixma, T.K., RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150 (2012), 1182–1195.
43. Meerang, M., Ritz, D., Paliwal, S., Garajova, Z., Bosshard, M., Mailand, N., Janscak, P., Hübscher, U., Meyer, H., Ramadan, K., The ubiquitin-selective segregase VCP/p97 orchestrates the response to DNA double-strand breaks. Nat. Cell Biol. 13 (2011), 1376–1382.
44. Meisenberg, C., Tait, P.S., Dianova, I.I., Wright, K., Edelmann, M.J., Ternette, N., Tasaki, T., Kessler, B.M., Parsons, J.L., Kwon, Y.T., Dianov, G.L., Ubiquitin ligase UBR3 regulates cellular levels of the essential DNA repair protein APE1 and is required for genome stability. Nucleic Acids Res. 40 (2012), 701–711.
45. Meisenberg, C., Ward, S.E., Schmid, P., El-Khamisy, S.F., TDP1/TOP1 ratio as a promising indicator for the response of small cell lung cancer to topotecan. J. Cancer Sci. Ther. 6 (2014), 258–267.
46. Meisenberg, C., Ashour, M.E., El-Shafie, L., Liao, C., Hodgson, A., Pilborough, A., Khurram, S.A., Downs, J.A., Ward, S.E., El-Khamisy, S.F., Epigenetic changes in histone acetylation underpin resistance to the topoisomerase I inhibitor irinotecan. Nucleic Acids Res. 45 (2017), 1159–1176.
47. Metzger, M.B., Pruneda, J.N., Klevit, R.E., Weissman, A.M., RING-type E3 ligases: master manipulators of E2 ubiquitin-conjugating enzymes and ubiquitination. Biochim. Biophys. Acta 1843 (2014), 47–60.
48. Miao, Z.-H., Agama, K., Sordet, O., Povirk, L., Kohn, K.W., Pommier, Y., Hereditary ataxia SCAN1 cells are defective for the repair of transcription-dependent topoisomerase I cleavage complexes. DNA Repair (Amst.) 5 (2006), 1489–1494.
49. Parsons, J.L., Tait, P.S., Finch, D., Dianova, I.I., Allinson, S.L., Dianov, G.L., CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. Mol. Cell 29 (2008), 477–487.
50. Parsons, J.L., Tait, P.S., Finch, D., Dianova, I.I., Edelmann, M.J., Khoronenkova, S.V., Kessler, B.M., Sharma, R.A., McKenna, W.G., Dianov, G.L., Ubiquitin ligase ARF-BP1/mule modulates base excision repair. EMBO J. 28 (2009), 3207–3215.
51. Pommier, Y., Sun, Y., Huang, S.N., Nitiss, J.L., Roles of eukaryotic topoisomerases in transcription, replication and genomic stability. Nat. Rev. Mol. Cell Biol. 17 (2016), 703–721.
52. Rehman, I., Basu, S.M., Das, S.K., Bhattacharjee, S., Ghosh, A., Pommier, Y., Das, B.B., PRMT5-mediated arginine methylation of TDP1 for the repair of topoisomerase I covalent complexes. Nucleic Acids Res., 2018, 10.1093/nar/gky291 Published online April 30.
53. Ritchie, M.E., Phipson, B., Wu, D., Hu, Y., Law, C.W., Shi, W., Smyth, G.K., limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res., 43, 2015, e47.
54. Rubinsztein, D.C., The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443 (2006), 780–786.
55. Sano, Y., Furuta, A., Setsuie, R., Kikuchi, H., Wang, Y.-L., Sakurai, M., Kwon, J., Noda, M., Wada, K., Photoreceptor cell apoptosis in the retinal degeneration of Uchl3-deficient mice. Am. J. Pathol. 169 (2006), 132–141.
56. Schellenberg, M.J., Lieberman, J.A., Herrero-Ruiz, A., Butler, L.R., Williams, J.G., Muñoz-Cabello, A.M., Mueller, G.A., London, R.E., Cortés-Ledesma, F., Williams, R.S., ZATT (ZNF451)-mediated resolution of topoisomerase 2 DNA-protein cross-links. Science 357 (2017), 1412–1416.
57. Setsuie, R., Sakurai, M., Sakaguchi, Y., Wada, K., Ubiquitin dimers control the hydrolase activity of UCH-L3. Neurochem. Int. 54 (2009), 314–321.
58. Setsuie, R., Suzuki, M., Tsuchiya, Y., Wada, K., Skeletal muscles of Uchl3 knockout mice show polyubiquitinated protein accumulation and stress responses. Neurochem. Int. 56 (2010), 911–918.
59. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J.R., Cole, P.A., Casero, R.A., Shi, Y., Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119 (2004), 941–953.
60. Smyth, G.K., Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol., 3, 2004, e3.
61. Takashima, H., Boerkoel, C.F., John, J., Saifi, G.M., Salih, M.A.M., Armstrong, D., Mao, Y., Quiocho, F.A., Roa, B.B., Nakagawa, M., et al. Mutation of TDP1, encoding a topoisomerase I-dependent DNA damage repair enzyme, in spinocerebellar ataxia with axonal neuropathy. Nat. Genet. 32 (2002), 267–272.
62. Trewick, S.C., Henshaw, T.F., Hausinger, R.P., Lindahl, T., Sedgwick, B., Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 419 (2002), 174–178.
63. van Cuijk, L., Vermeulen, W., Marteijn, J.A., Ubiquitin at work: the ubiquitous regulation of the damage recognition step of NER. Exp. Cell Res. 329 (2014), 101–109.
64. Vaz, B., Popovic, M., Newman, J.A., Fielden, J., Aitkenhead, H., Halder, S., Singh, A.N., Vendrell, I., Fischer, R., Torrecilla, I., et al. Metalloprotease SPRTN/DVC1 orchestrates replication-coupled DNA-protein crosslink repair. Mol. Cell 64 (2016), 704–719.
65. Walker, C., El-Khamisy, S.F., Perturbed autophagy and DNA repair converge to promote neurodegeneration in amyotrophic lateral sclerosis and dementia. Brain 141 (2018), 1247–1262.
66. Walker, C., Herranz-Martin, S., Karyka, E., Liao, C., Lewis, K., Elsayed, W., Lukashchuk, V., Chiang, S.-C., Ray, S., Mulcahy, P.J., et al. C9orf72 expansion disrupts ATM-mediated chromosomal break repair. Nat. Neurosci. 20 (2017), 1225–1235.
67. Wang, Q., Liu, Y., Zou, X., Wang, Q., An, M., Guan, X., He, J., Tong, Y., Ji, J., The hippocampal proteomic analysis of senescence-accelerated mouse: implications of Uchl3 and mitofilin in cognitive disorder and mitochondria dysfunction in SAMP8. Neurochem. Res. 33 (2008), 1776–1782.
68. Wilson, M.D., Saponaro, M., Leidl, M.A., Svejstrup, J.Q., MultiDsk: a ubiquitin-specific affinity resin. PLoS ONE, 7, 2012, e46398.
69. Wood, M.A., Kaplan, M.P., Brensinger, C.M., Guo, W., Abel, T., Ubiquitin C-terminal hydrolase L3 (Uchl3) is involved in working memory. Hippocampus 15 (2005), 610–621.
70. Zhang, Y., Zhou, L., Rouge, L., Phillips, A.H., Lam, C., Liu, P., Sandoval, W., Helgason, E., Murray, J.M., Wertz, I.E., Corn, J.E., Conformational stabilization of ubiquitin yields potent and selective inhibitors of USP7. Nat. Chem. Biol. 9 (2013), 51–58.
71. Zhou, T., Lee, J.W., Tatavarthi, H., Lupski, J.R., Valerie, K., Povirk, L.F., Deficiency in 3′-phosphoglycolate processing in human cells with a hereditary mutation in tyrosyl-DNA phosphodiesterase (TDP1). Nucleic Acids Res. 33 (2005), 289–297.