Autophagy Regulates Chromatin Ubiquitination in DNA Damage Response through Elimination of SQSTM1/p62

Molecular Cell

Volumn 63, Issue 1, 2016, Pages 34-48

  Wang, Yanan ^a   Zhang, Nan ^a   Zhang, Luyao ^a   Li, Ran ^a   Fu, Wan ^a   Ma, Ke ^a   Li, Xue ^a   Wang, Lina ^a   Wang, Jiadong ^a   Zhang, Hongquan ^a   Gu, Wei ^b   Zhu, Wei Guo ^a,c   Zhao, Ying ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b Columbia University ^*  (United States)

^c Shenzhen University School of Medicine   (China)

Author keywords

autophagy; DNA damage; histone ubiquitination; p62

Indexed keywords

AUTOPHAGIC CARGO RECEPTOR; BRCA1 PROTEIN; DOUBLE STRANDED DNA; E3 LIGASE RNF168; HISTONE H2A; HISTONE H2B; NUCLEIC ACID BINDING PROTEIN; PROTEIN P62; RAD51 PROTEIN; RAP80 PROTEIN; RECEPTOR; SQSTM1 PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ATG3 PROTEIN, HUMAN; AUTOPHAGY RELATED PROTEIN; CHROMATIN; HISTONE; RNF168 PROTEIN, HUMAN; SEQUESTOSOME 1; SQSTM1 PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE;

ANIMAL CARE; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CANCER RADIOTHERAPY; CELL SURVIVAL; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE RESPONSE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; FEMALE; HELA CELL LINE; HISTONE UBIQUITINATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PROTEIN PROTEIN INTERACTION; RADIOSENSITIVITY; REGULATORY MECHANISM; CHROMATIN ASSEMBLY AND DISASSEMBLY; COLORECTAL NEOPLASMS; GENETIC TRANSFECTION; GENETICS; HCT 116 CELL LINE; METABOLISM; PATHOLOGY; RADIATION RESPONSE; RADIATION TOLERANCE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UBIQUITINATION;

AUTOPHAGY; AUTOPHAGY-RELATED PROTEINS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; COLORECTAL NEOPLASMS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; HCT116 CELLS; HISTONES; HUMANS; RADIATION TOLERANCE; RNA INTERFERENCE; SEQUESTOSOME-1 PROTEIN; SIGNAL TRANSDUCTION; TRANSFECTION; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84992435551     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.05.027     Document Type: Article

References (53)

1. Bjørkøy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., Stenmark, H., Johansen, T., p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171 (2005), 603–614.
2. Chen, S., Wang, C., Sun, L., Wang, D.L., Chen, L., Huang, Z., Yang, Q., Gao, J., Yang, X.B., Chang, J.F., et al. RAD6 promotes homologous recombination repair by activating the autophagy-mediated degradation of heterochromatin protein HP1. Mol. Cell. Biol. 35 (2015), 406–416.
3. Clausen, T.H., Lamark, T., Isakson, P., Finley, K., Larsen, K.B., Brech, A., Øvervatn, A., Stenmark, H., Bjørkøy, G., Simonsen, A., Johansen, T., p62/SQSTM1 and ALFY interact to facilitate the formation of p62 bodies/ALIS and their degradation by autophagy. Autophagy 6 (2010), 330–344.
4. 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.
5. Fan, W., Tang, Z., Chen, D., Moughon, D., Ding, X., Chen, S., Zhu, M., Zhong, Q., Keap1 facilitates p62-mediated ubiquitin aggregate clearance via autophagy. Autophagy 6 (2010), 614–621.
6. Feng, L., Chen, J., The E3 ligase RNF8 regulates KU80 removal and NHEJ repair. Nat. Struct. Mol. Biol. 19 (2012), 201–206.
7. Feng, Y., Longmore, G.D., The LIM protein Ajuba influences interleukin-1-induced NF-kappaB activation by affecting the assembly and activity of the protein kinase Czeta/p62/TRAF6 signaling complex. Mol. Cell. Biol. 25 (2005), 4010–4022.
8. Filimonenko, M., Isakson, P., Finley, K.D., Anderson, M., Jeong, H., Melia, T.J., Bartlett, B.J., Myers, K.M., Birkeland, H.C., Lamark, T., et al. The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein Alfy. Mol. Cell 38 (2010), 265–279.
9. Green, D.R., Levine, B., To be or not to be? How selective autophagy and cell death govern cell fate. Cell 157 (2014), 65–75.
10. Huen, M.S., 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.
11. Ichimura, Y., Kumanomidou, T., Sou, Y.S., Mizushima, T., Ezaki, J., Ueno, T., Kominami, E., Yamane, T., Tanaka, K., Komatsu, M., Structural basis for sorting mechanism of p62 in selective autophagy. J. Biol. Chem. 283 (2008), 22847–22857.
12. Itakura, E., Mizushima, N., p62 Targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding. J. Cell Biol. 192 (2011), 17–27.
13. Jain, A., Lamark, T., Sjøttem, E., Larsen, K.B., Awuh, J.A., Øvervatn, A., McMahon, M., Hayes, J.D., Johansen, T., p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J. Biol. Chem. 285 (2010), 22576–22591.
14. Karantza-Wadsworth, V., Patel, S., Kravchuk, O., Chen, G., Mathew, R., Jin, S., White, E., Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev. 21 (2007), 1621–1635.
15. Kim, H., Chen, J., Yu, X., Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316 (2007), 1202–1205.
16. Kirkin, V., Lamark, T., Sou, Y.S., Bjørkøy, G., Nunn, J.L., Bruun, J.A., Shvets, E., McEwan, D.G., Clausen, T.H., Wild, P., et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 33 (2009), 505–516.
17. Klionsky, D.J., Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 8 (2007), 931–937.
18. Kolas, N.K., Chapman, J.R., Nakada, S., Ylanko, J., Chahwan, R., Sweeney, F.D., Panier, S., Mendez, M., Wildenhain, J., Thomson, T.M., et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318 (2007), 1637–1640.
19. Komatsu, M., Waguri, S., Koike, M., Sou, Y.S., Ueno, T., Hara, T., Mizushima, N., Iwata, J., Ezaki, J., Murata, S., et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131 (2007), 1149–1163.
20. Komatsu, M., Kurokawa, H., Waguri, S., Taguchi, K., Kobayashi, A., Ichimura, Y., Sou, Y.S., Ueno, I., Sakamoto, A., Tong, K.I., et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 12 (2010), 213–223.
21. Kuusisto, E., Salminen, A., Alafuzoff, I., Ubiquitin-binding protein p62 is present in neuronal and glial inclusions in human tauopathies and synucleinopathies. Neuroreport 12 (2001), 2085–2090.
22. Lau, A., Wang, X.J., Zhao, F., Villeneuve, N.F., Wu, T., Jiang, T., Sun, Z., White, E., Zhang, D.D., A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol. Cell. Biol. 30 (2010), 3275–3285.
23. Liu, E.Y., Xu, N., O'Prey, J., Lao, L.Y., Joshi, S., Long, J.S., O'Prey, M., Croft, D.R., Beaumatin, F., Baudot, A.D., et al. Loss of autophagy causes a synthetic lethal deficiency in DNA repair. Proc. Natl. Acad. Sci. USA 112 (2015), 773–778.
24. 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.
25. Mathew, R., Karantza-Wadsworth, V., White, E., Role of autophagy in cancer. Nat. Rev. Cancer 7 (2007), 961–967.
26. Mathew, R., Kongara, S., Beaudoin, B., Karp, C.M., Bray, K., Degenhardt, K., Chen, G., Jin, S., White, E., Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev. 21 (2007), 1367–1381.
27. Mathew, R., Karp, C.M., Beaudoin, B., Vuong, N., Chen, G., Chen, H.Y., Bray, K., Reddy, A., Bhanot, G., Gelinas, C., et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 137 (2009), 1062–1075.
28. Mattiroli, F., Vissers, J.H., 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.
29. Mattiroli, F., Uckelmann, M., Sahtoe, D.D., van Dijk, W.J., Sixma, T.K., The nucleosome acidic patch plays a critical role in RNF168-dependent ubiquitination of histone H2A. Nat. Commun., 5, 2014, 3291.
30. Middleton, A.J., Budhidarmo, R., Day, C.L., Use of E2∼ubiquitin conjugates for the characterization of ubiquitin transfer by RING E3 ligases such as the inhibitor of apoptosis proteins. Methods Enzymol. 545 (2014), 243–263.
31. Mizushima, N., Autophagy in protein and organelle turnover. Cold Spring Harb. Symp. Quant. Biol. 76 (2011), 397–402.
32. Mizushima, N., Komatsu, M., Autophagy: renovation of cells and tissues. Cell 147 (2011), 728–741.
33. Mizushima, N., Levine, B., Cuervo, A.M., Klionsky, D.J., Autophagy fights disease through cellular self-digestion. Nature 451 (2008), 1069–1075.
34. Mortensen, M., Soilleux, E.J., Djordjevic, G., Tripp, R., Lutteropp, M., Sadighi-Akha, E., Stranks, A.J., Glanville, J., Knight, S., Jacobsen, S.E., et al. The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance. J. Exp. Med. 208 (2011), 455–467.
35. Nakada, S., Tai, I., Panier, S., Al-Hakim, A., Iemura, S., Juang, Y.C., O'Donnell, L., Kumakubo, A., Munro, M., Sicheri, F., et al. Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 466 (2010), 941–946.
36. Nezis, I.P., Simonsen, A., Sagona, A.P., Finley, K., Gaumer, S., Contamine, D., Rusten, T.E., Stenmark, H., Brech, A., Ref(2)P, the Drosophila melanogaster homologue of mammalian p62, is required for the formation of protein aggregates in adult brain. J. Cell Biol. 180 (2008), 1065–1071.
37. Okamoto, K., Organellophagy: eliminating cellular building blocks via selective autophagy. J. Cell Biol. 205 (2014), 435–445.
38. Panier, S., Ichijima, Y., Fradet-Turcotte, A., Leung, C.C., Kaustov, L., Arrowsmith, C.H., Durocher, D., Tandem protein interaction modules organize the ubiquitin-dependent response to DNA double-strand breaks. Mol. Cell 47 (2012), 383–395.
39. Pankiv, S., Clausen, T.H., Lamark, T., Brech, A., Bruun, J.A., Outzen, H., Øvervatn, A., Bjørkøy, G., Johansen, T., p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282 (2007), 24131–24145.
40. Pankiv, S., Lamark, T., Bruun, J.A., Øvervatn, A., Bjørkøy, G., Johansen, T., Nucleocytoplasmic shuttling of p62/SQSTM1 and its role in recruitment of nuclear polyubiquitinated proteins to promyelocytic leukemia bodies. J. Biol. Chem. 285 (2010), 5941–5953.
41. Rello-Varona, S., Lissa, D., Shen, S., Niso-Santano, M., Senovilla, L., Mariño, G., Vitale, I., Jemaá, M., Harper, F., Pierron, G., et al. Autophagic removal of micronuclei. Cell Cycle 11 (2012), 170–176.
42. Sancar, A., Lindsey-Boltz, L.A., Unsal-Kaçmaz, K., Linn, S., Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73 (2004), 39–85.
43. Sobhian, B., Shao, G., Lilli, D.R., Culhane, A.C., Moreau, L.A., Xia, B., Livingston, D.M., Greenberg, R.A., RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316 (2007), 1198–1202.
44. Sonoda, E., Hochegger, H., Saberi, A., Taniguchi, Y., Takeda, S., Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst.) 5 (2006), 1021–1029.
45. Stewart, G.S., Stankovic, T., Byrd, P.J., Wechsler, T., Miller, E.S., Huissoon, A., Drayson, M.T., West, S.C., Elledge, S.J., Taylor, A.M., RIDDLE immunodeficiency syndrome is linked to defects in 53BP1-mediated DNA damage signaling. Proc. Natl. Acad. Sci. USA 104 (2007), 16910–16915.
46. Stewart, G.S., Panier, S., Townsend, K., Al-Hakim, A.K., Kolas, N.K., Miller, E.S., Nakada, S., Ylanko, J., Olivarius, S., Mendez, M., et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136 (2009), 420–434.
47. Stolz, A., Ernst, A., Dikic, I., Cargo recognition and trafficking in selective autophagy. Nat. Cell Biol. 16 (2014), 495–501.
48. Stumptner, C., Fuchsbichler, A., Heid, H., Zatloukal, K., Denk, H., Mallory body—a disease-associated type of sequestosome. Hepatology 35 (2002), 1053–1062.
49. Thorslund, T., Ripplinger, A., Hoffmann, S., Wild, T., Uckelmann, M., Villumsen, B., Narita, T., Sixma, T.K., Choudhary, C., Bekker-Jensen, S., Mailand, N., Histone H1 couples initiation and amplification of ubiquitin signalling after DNA damage. Nature 527 (2015), 389–393.
50. Wang, B., Elledge, S.J., Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc. Natl. Acad. Sci. USA 104 (2007), 20759–20763.
51. Wang, B., Matsuoka, S., Ballif, B.A., Zhang, D., Smogorzewska, A., Gygi, S.P., Elledge, S.J., Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316 (2007), 1194–1198.
52. Wright, J.D., Mace, P.D., Day, C.L., Secondary ubiquitin-RING docking enhances Arkadia and Ark2C E3 ligase activity. Nat. Struct. Mol. Biol. 23 (2016), 45–52.
53. Zatloukal, K., Stumptner, C., Fuchsbichler, A., Heid, H., Schnoelzer, M., Kenner, L., Kleinert, R., Prinz, M., Aguzzi, A., Denk, H., p62 Is a common component of cytoplasmic inclusions in protein aggregation diseases. Am. J. Pathol. 160 (2002), 255–263.