Please note this is a comparison between Version 2 by Vivi Li and Version 1 by Katharina Witting.
Post-translational modification with Ubiquitin-like proteins represents a complex signaling language regulating virtually every cellular process. Among these post-translational modifiers is Ubiquitin-fold modifier (UFM1), which is covalently attached to its substrates through the orchestrated action of a dedicated enzymatic cascade. Originally identified to be involved embryonic development, its biological function remains enigmatic. Recent research reveals that UFM1 regulates a variety of cellular events ranging from DNA repair to autophagy and ER stress response implicating its involvement in a variety of diseases. Given the contribution of UFM1 to numerous pathologies, the enzymes of the UFM1 cascade represent attractive targets for pharmacological inhibition.
UFM1
Ubiquitin-like modifiers
substrates
activity-based probes
Please wait, diff process is still running!
References
Wei, Y.; Xu, X. UFMylation: A Unique & Fashionable Modification for Life. Genom. Proteom. Bioinform. 2016, 14, 140–146.
Schulman, B.A.; Harper, J.W. Ubiquitin-like protein activation by E1 enzymes: The apex for downstream signalling pathways. Nat. Rev. Mol. Cell Biol. 2009, 10, 319–331.
Padala, P.; Oweis, W.; Mashahreh, B.; Soudah, N.; Cohen-Kfir, E.; Todd, E.A.; Berndsen, C.E.; Wiener, R. Novel insights into the interaction of UBA5 with UFM1 via a UFM1-interacting sequence. Sci. Rep. 2017, 7, 508.
Habisov, S.; Huber, J.; Ichimura, Y.; Akutsu, M.; Rogova, N.; Loehr, F.; McEwan, D.G.; Johansen, T.; Dikic, I.; Doetsch, V.; et al. Structural and Functional Analysis of a Novel Interaction Motif within UFM1-activating Enzyme 5 (UBA5) Required for Binding to Ubiquitin-like Proteins and Ufmylation. J. Biol. Chem. 2016, 291, 9025–9041.
Soudah, N.; Padala, P.; Hassouna, F.; Kumar, M.; Mashahreh, B.; Lebedev, A.A.; Isupov, M.N.; Cohen-Kfir, E.; Wiener, R. An N-Terminal Extension to UBA5 Adenylation Domain Boosts UFM1 Activation: Isoform-Specific Differences in Ubiquitin-like Protein Activation. J. Mol. Biol. 2019, 431, 463–478.
Lv, Z.; Olsen, S.K. UFM1-Activating Enzyme 5 (Uba5) Requires an Extension to Get the Job Done Right. J. Mol. Biol. 2019, 431, 479–482.
Bacik, J.P.; Walker, J.R.; Ali, M.; Schimmer, A.D.; Dhe-Paganon, S. Crystal structure of the human ubiquitin-activating enzyme 5 (UBA5) bound to ATP: Mechanistic insights into a minimalistic E1 enzyme. J. Biol. Chem. 2010, 285, 20273–20280.
Gavin, J.M.; Hoar, K.; Xu, Q.; Ma, J.; Lin, Y.; Chen, J.; Chen, W.; Bruzzese, F.J.; Harrison, S.; Mallender, W.D.; et al. Mechanistic study of Uba5 enzyme and the Ufm1 conjugation pathway. J. Biol. Chem. 2014, 289, 22648–22658.
Mashahreh, B.; Hassouna, F.; Soudah, N.; Cohen-Kfir, E.; Strulovich, R.; Haitin, Y.; Wiener, R. Trans-binding of UFM1 to UBA5 stimulates UBA5 homodimerization and ATP binding. FASEB J. 2018, 32, 2794–2802.
Huber, J.; Obata, M.; Gruber, J.; Akutsu, M.; Lohr, F.; Rogova, N.; Guntert, P.; Dikic, I.; Kirkin, V.; Komatsu, M.; et al. An atypical LIR motif within UBA5 (ubiquitin like modifier activating enzyme 5) interacts with GABARAP proteins and mediates membrane localization of UBA5. Autophagy 2020, 16, 256–270.
Ishimura, R.; Obata, M.; Kageyama, S.; Daniel, J.; Tanaka, K.; Komatsu, M. A novel approach to assess the ubiquitin-fold modifier 1-system in cells. FEBS Lett. 2017, 591, 196–204.
Komatsu, M.; Chiba, T.; Tatsumi, K.; Iemura, S.; Tanida, I.; Okazaki, N.; Ueno, T.; Kominami, E.; Natsume, T.; Tanaka, K. A novel protein-conjugating system for Ufm1, a ubiquitin-fold modifier. EMBO J. 2004, 23, 1977–1986.
Mizushima, T.; Tatsumi, K.; Ozaki, Y.; Kawakami, T.; Suzuki, A.; Ogasahara, K.; Komatsu, M.; Kominami, E.; Tanaka, K.; Yamane, T. Crystal structure of Ufc1, the Ufm1-conjugating enzyme. Biochem. Biophys. Res. Commun. 2007, 362, 1079–1084.
Liu, G.; Aramini, J.; Atreya, H.S.; Eletsky, A.; Xiao, R.; Acton, T.; Ma, L.; Montelione, G.T.; Szyperski, T. GFT NMR based resonance assignment for the 21 kDa human protein UFC1. J. Biomol. NMR 2005, 32, 261.
Liu, G.; Forouhar, F.; Eletsky, A.; Atreya, H.S.; Aramini, J.M.; Xiao, R.; Huang, Y.J.; Abashidze, M.; Seetharaman, J.; Liu, J.; et al. NMR and X-RAY structures of human E2-like ubiquitin-fold modifier conjugating enzyme 1 (UFC1) reveal structural and functional conservation in the metazoan UFM1-UBA5-UFC1 ubiquination pathway. J. Struct. Funct. Genom. 2009, 10, 127–136.
Xie, S. Characterization, crystallization and preliminary X-ray crystallographic analysis of the human Uba5 C-terminus-Ufc1 complex. Acta Crystallogr. F Struct. Biol. Commun. 2014, 70, 1093–1097.
Daniel, J.; Liebau, E. The ufm1 cascade. Cells 2014, 3, 627–638.
Xie, Z.; Fang, Z.; Pan, Z. Ufl1/RCAD, a Ufm1 E3 ligase, has an intricate connection with ER stress. Int. J. Biol. Macromol. 2019, 135, 760–767.
Tatsumi, K.; Sou, Y.S.; Tada, N.; Nakamura, E.; Iemura, S.; Natsume, T.; Kang, S.H.; Chung, C.H.; Kasahara, M.; Kominami, E.; et al. A novel type of E3 ligase for the Ufm1 conjugation system. J. Biol. Chem. 2010, 285, 5417–5427.
Lemaire, K.; Moura, R.F.; Granvik, M.; Igoillo-Esteve, M.; Hohmeier, H.E.; Hendrickx, N.; Newgard, C.B.; Waelkens, E.; Cnop, M.; Schuit, F. Ubiquitin fold modifier 1 (UFM1) and its target UFBP1 protect pancreatic beta cells from ER stress-induced apoptosis. PLoS ONE 2011, 6, e18517.
Yoo, H.M.; Kang, S.H.; Kim, J.Y.; Lee, J.E.; Seong, M.W.; Lee, S.W.; Ka, S.H.; Sou, Y.S.; Komatsu, M.; Tanaka, K.; et al. Modification of ASC1 by UFM1 is crucial for ERalpha transactivation and breast cancer development. Mol. Cell 2014, 56, 261–274.
Walczak, C.P.; Leto, D.E.; Zhang, L.; Riepe, C.; Muller, R.Y.; DaRosa, P.A.; Ingolia, N.T.; Elias, J.E.; Kopito, R.R. Ribosomal protein RPL26 is the principal target of UFMylation. Proc. Natl. Acad. Sci. USA 2019, 116, 1299–1308.
Wang, L.; Xu, Y.; Rogers, H.; Saidi, L.; Noguchi, C.T.; Li, H.; Yewdell, J.W.; Guydosh, N.R.; Ye, Y. UFMylation of RPL26 links translocation-associated quality control to endoplasmic reticulum protein homeostasis. Cell Res. 2020, 30, 5–20.
Scheel, H.; Hofmann, K. Prediction of a common structural scaffold for proteasome lid, COP9-signalosome and eIF3 complexes. BMC Bioinform. 2005, 6, 71.
Liang, J.R.; Lingeman, E.; Luong, T.; Ahmed, S.; Muhar, M.; Nguyen, T.; Olzmann, J.A.; Corn, J.E. A Genome-wide ER-phagy Screen Highlights Key Roles of Mitochondrial Metabolism and ER-Resident UFMylation. Cell 2020, 180, 1160–1177.
Duda, D.M.; Borg, L.A.; Scott, D.C.; Hunt, H.W.; Hammel, M.; Schulman, B.A. Structural insights into NEDD8 activation of cullin-RING ligases: Conformational control of conjugation. Cell 2008, 134, 995–1006.
Mak, G.W.; Lai, W.L.; Zhou, Y.; Li, M.; Ng, I.O.; Ching, Y.P. CDK5RAP3 is a novel repressor of p14ARF in hepatocellular carcinoma cells. PLoS ONE 2012, 7, e42210.
Jiang, H.; Wu, J.; He, C.; Yang, W.; Li, H. Tumor suppressor protein C53 antagonizes checkpoint kinases to promote cyclin-dependent kinase 1 activation. Cell Res. 2009, 19, 458–468.
Jiang, H.; Luo, S.; Li, H. Cdk5 activator-binding protein C53 regulates apoptosis induced by genotoxic stress via modulating the G2/M DNA damage checkpoint. J. Biol. Chem. 2005, 280, 20651–20659.
Kwon, J.; Cho, H.J.; Han, S.H.; No, J.G.; Kwon, J.Y.; Kim, H. A novel LZAP-binding protein, NLBP, inhibits cell invasion. J. Biol. Chem. 2010, 285, 12232–12240.
Shiwaku, H.; Yoshimura, N.; Tamura, T.; Sone, M.; Ogishima, S.; Watase, K.; Tagawa, K.; Okazawa, H. Suppression of the novel ER protein Maxer by mutant ataxin-1 in Bergman glia contributes to non-cell-autonomous toxicity. EMBO J. 2010, 29, 2446–2460.
Wu, J.; Lei, G.; Mei, M.; Tang, Y.; Li, H. A novel C53/LZAP-interacting protein regulates stability of C53/LZAP and DDRGK domain-containing Protein 1 (DDRGK1) and modulates NF-kappaB signaling. J. Biol. Chem. 2010, 285, 15126–15136.
Yang, R.; Wang, H.; Kang, B.; Chen, B.; Shi, Y.; Yang, S.; Sun, L.; Liu, Y.; Xiao, W.; Zhang, T.; et al. CDK5RAP3, a UFL1 substrate adaptor, is crucial for liver development. Development 2019, 146, dev169235.
Kang, S.H.; Kim, G.R.; Seong, M.; Baek, S.H.; Seol, J.H.; Bang, O.S.; Ovaa, H.; Tatsumi, K.; Komatsu, M.; Tanaka, K.; et al. Two novel ubiquitin-fold modifier 1 (Ufm1)-specific proteases, UfSP1 and UfSP2. J. Biol. Chem. 2007, 282, 5256–5262.
Ha, B.H.; Ahn, H.C.; Kang, S.H.; Tanaka, K.; Chung, C.H.; Kim, E.E. Structural basis for Ufm1 processing by UfSP1. J. Biol. Chem. 2008, 283, 14893–14900.
Ha, B.H.; Jeon, Y.J.; Shin, S.C.; Tatsumi, K.; Komatsu, M.; Tanaka, K.; Watson, C.M.; Wallis, G.; Chung, C.H.; Kim, E.E. Structure of ubiquitin-fold modifier 1-specific protease UfSP2. J. Biol. Chem. 2011, 286, 10248–10257.
Witting, K.F.; van Noort, G.J.v.d.H.; Kofoed, C.; Ormeno, C.T.; Atmioui, D.E.; Mulder, M.P.C.; Ovaa, H. Generation of the UFM1 Toolkit for Profiling UFM1-Specific Proteases and Ligases. Angew. Chem. Int. Ed. Engl. 2018, 57, 14164–14168.
Gerakis, Y.; Quintero, M.; Li, H.; Hetz, C. The UFMylation System in Proteostasis and Beyond. Trends Cell Biol. 2019, 29, 974–986.
Cai, Y.; Singh, N.; Li, H. Essential role of Ufm1 conjugation in the hematopoietic system. Exp. Hematol. 2016, 44, 442–446.
Zhang, Y.; Zhang, M.; Wu, J.; Lei, G.; Li, H. Transcriptional regulation of the Ufm1 conjugation system in response to disturbance of the endoplasmic reticulum homeostasis and inhibition of vesicle trafficking. PLoS ONE 2012, 7, e48587.
Merbl, Y.; Refour, P.; Patel, H.; Springer, M.; Kirschner, M.W. Profiling of ubiquitin-like modifications reveals features of mitotic control. Cell 2013, 152, 1160–1172.
Eck, F.; Phuyal, S.; Smith, M.D.; Kaulich, M.; Wilkinson, S.; Farhan, H.; Behrends, C. ACSL3 is a novel GABARAPL2 interactor that links ufmylation and lipid droplet biogenesis. J. Cell Sci. 2020, 133, jcs243477.
Lin, J.X.; Xie, X.S.; Weng, X.F.; Qiu, S.L.; Yoon, C.; Lian, N.Z.; Xie, J.W.; Wang, J.B.; Lu, J.; Chen, Q.Y.; et al. UFM1 suppresses invasive activities of gastric cancer cells by attenuating the expres7sion of PDK1 through PI3K/AKT signaling. J. Exp. Clin. Cancer Res. 2019, 38, 410.
Liu, J.; Guan, D.; Dong, M.; Yang, J.; Wei, H.; Liang, Q.; Song, L.; Xu, L.; Bai, J.; Liu, C.; et al. UFMylation maintains tumour suppressor p53 stability by antagonizing its ubiquitination. Nat. Cell Biol. 2020, 22, 1056–1063.
De Jesus, R.; Moretti, F.; McAllister, G.; Wang, Z.; Bergman, P.; Liu, S.; Frias, E.; Alford, J.; Reece-Hoyes, J.S.; Lindeman, A.; et al. Functional CRISPR screening identifies the ufmylation pathway as a regulator of SQSTM1/p62. Elife 2016, 5, e17290.
Tatsumi, K.; Yamamoto-Mukai, H.; Shimizu, R.; Waguri, S.; Sou, Y.S.; Sakamoto, A.; Taya, C.; Shitara, H.; Hara, T.; Chung, C.H.; et al. The Ufm1-activating enzyme Uba5 is indispensable for erythroid differentiation in mice. Nat. Commun. 2011, 2, 181.
Cai, Y.; Pi, W.; Sivaprakasam, S.; Zhu, X.; Zhang, M.; Chen, J.; Makala, L.; Lu, C.; Wu, J.; Teng, Y.; et al. UFBP1, a Key Component of the Ufm1 Conjugation System, Is Essential for Ufmylation-Mediated Regulation of Erythroid Development. PLoS Genet. 2015, 11, e1005643.
Zhang, M.; Zhu, X.; Zhang, Y.; Cai, Y.; Chen, J.; Sivaprakasam, S.; Gurav, A.; Pi, W.; Makala, L.; Wu, J.; et al. RCAD/Ufl1, a Ufm1 E3 ligase, is essential for hematopoietic stem cell function and murine hematopoiesis. Cell Death Differ. 2015, 22, 1922–1934.
Liu, J.; Wang, Y.; Song, L.; Zeng, L.; Yi, W.; Liu, T.; Chen, H.; Wang, M.; Ju, Z.; Cong, Y.S. A critical role of DDRGK1 in endoplasmic reticulum homoeostasis via regulation of IRE1alpha stability. Nat. Commun. 2017, 8, 14186.
Cai, Y.; Zhu, G.; Liu, S.; Pan, Z.; Quintero, M.; Poole, C.J.; Lu, C.; Zhu, H.; Islam, B.; Riggelen, J.V.; et al. Indispensable role of the Ubiquitin-fold modifier 1-specific E3 ligase in maintaining intestinal homeostasis and controlling gut inflammation. Cell Discov. 2019, 5, 7.
Lin, K.Y.; Kao, S.H.; Lai, C.M.; Chen, C.T.; Wu, C.Y.; Hsu, H.J.; Wang, W.D. Tumor Suppressor Lzap Suppresses Wnt/beta-Catenin Signaling to Promote Zebrafish Embryonic Ventral Cell Fates via the Suppression of Inhibitory Phosphorylation of Glycogen Synthase Kinase 3. J. Biol. Chem. 2015, 290, 29808–29819.
Bruce, A.E.E.; Heisenberg, C.P. Mechanisms of zebrafish epiboly: A current view. Curr. Top. Dev. Biol. 2020, 136, 319–341.
Sharma, S.; Sicinski, P. A kinase of many talents: Non-neuronal functions of CDK5 in development and disease. Open Biol. 2020, 10, 190287.
Stephani, M.; Picchianti, L.; Dagdas, Y. C53 is a cross-kingdom conserved reticulophagy receptor that bridges the gap betweenselective autophagy and ribosome stalling at the endoplasmic reticulum. Autophagy 2020, 1–2.
Ching, Y.P.; Qi, Z.; Wang, J.H. Cloning of three novel neuronal Cdk5 activator binding proteins. Gene 2000, 242, 285–294.
Neziri, D.; Ilhan, A.; Maj, M.; Majdic, O.; Baumgartner-Parzer, S.; Cohen, G.; Base, W.; Wagner, L. Cloning and molecular characterization of Dashurin encoded by C20orf116, a PCI-domain containing protein. Biochim. Biophys. Acta 2010, 1800, 430–438.
Hetz, C. The unfolded protein response: Controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 2012, 13, 89–102.
Chen, X.; Karnovsky, A.; Sans, M.D.; Andrews, P.C.; Williams, J.A. Molecular characterization of the endoplasmic reticulum: Insights from proteomic studies. Proteomics 2010, 10, 4040–4052.
Rashid, H.O.; Yadav, R.K.; Kim, H.R.; Chae, H.J. ER stress: Autophagy induction, inhibition and selection. Autophagy 2015, 11, 1956–1977.
Azfer, A.; Niu, J.; Rogers, L.M.; Adamski, F.M.; Kolattukudy, P.E. Activation of endoplasmic reticulum stress response during the development of ischemic heart disease. Am. J. Physiol. Heart Circ. Physiol. 2006, 291, H1411–H1420.
Zhu, Y.; Lei, Q.; Li, D.; Zhang, Y.; Jiang, X.; Hu, Z.; Xu, G. Proteomic and Biochemical Analyses Reveal a Novel Mechanism for Promoting Protein Ubiquitination and Degradation by UFBP1, a Key Component of Ufmylation. J. Proteome Res. 2018, 17, 1509–1520.
Sun, S.; Shi, G.; Sha, H.; Ji, Y.; Han, X.; Shu, X.; Ma, H.; Inoue, T.; Gao, B.; Kim, H.; et al. IRE1alpha is an endogenous substrate of endoplasmic-reticulum-associated degradation. Nat. Cell Biol. 2015, 17, 1546–1555.
Bagola, K.; Mehnert, M.; Jarosch, E.; Sommer, T. Protein dislocation from the ER. Biochim. Biophys. Acta 2011, 1808, 925–936.
Simsek, D.; Tiu, G.C.; Flynn, R.A.; Byeon, G.W.; Leppek, K.; Xu, A.F.; Chang, H.Y.; Barna, M. The Mammalian Ribo-interactome Reveals Ribosome Functional Diversity and Heterogeneity. Cell 2017, 169, 1051–1065.
Wang, S.; Jia, M.; Su, M.; Hu, X.; Li, J.; Xu, Y.; Qiu, W. Ufmylation Is Activated in Renal Cancer and Is Not Associated with von Hippel-Lindau Mutation. DNA Cell Biol. 2020, 39, 654–660.
Schuren, A.B.C.; Boer, I.G.J.; Bouma, E.M.; Van de Weijer, M.L.; Costa, A.I.; Hubel, P.; Pichlmair, A.; Lebbink, R.J.; Wiertz, E. The UFM1 Pathway Impacts HCMV US2-Mediated Degradation of HLA Class I. Molecules 2021, 26, 287.
Dikic, I.; Elazar, Z. Mechanism and medical implications of mammalian autophagy. Nat. Rev. Mol. Cell Biol. 2018, 19, 349–364.
Hu, X.; Zhang, H.; Song, Y.; Zhuang, L.; Yang, Q.; Pan, M.; Chen, F. Ubiquitin fold modifier 1 activates NF-kappaB pathway by down-regulating LZAP expression in the macrophage of diabetic mouse model. Biosci. Rep. 2020, 40, BSR20191672.
Miller, C.; Cai, Y.; Patton, T.; Graves, S.H.; Li, H.; Sabbatini, M.E. RCAD/BiP pathway is necessary for the proper synthesis of digestive enzymes and secretory function of the exocrine pancreas. Am. J. Physiol. Gastrointest. Liver Physiol. 2017, 312, G314–G326.
Johansen, T.; Lamark, T. Selective Autophagy: ATG8 Family Proteins, LIR Motifs and Cargo Receptors. J. Mol. Biol. 2020, 432, 80–103.
Stolz, A.; Ernst, A.; Dikic, I. Cargo recognition and trafficking in selective autophagy. Nat. Cell Biol. 2014, 16, 495–501.
Song, S.; Tan, J.; Miao, Y.; Zhang, Q. Crosstalk of ER stress-mediated autophagy and ER-phagy: Involvement of UPR and the core autophagy machinery. J. Cell Physiol. 2018, 233, 3867–3874.
Strzyz, P. Foundations of ER-phagy regulation. Nat. Rev. Mol. Cell Biol. 2020, 21, 251.
Jarc, E.; Petan, T. Lipid Droplets and the Management of Cellular Stress. Yale J. Biol. Med. 2019, 92, 435–452.
Homrich, M.; Wobst, H.; Laurini, C.; Sabrowski, J.; Schmitz, B.; Diestel, S. Cytoplasmic domain of NCAM140 interacts with ubiquitin-fold modifier-conjugating enzyme-1 (Ufc1). Exp. Cell Res. 2014, 324, 192–199.
Statello, L.; Guo, C.J.; Chen, L.L.; Huarte, M. Gene regulation by long non-coding RNAs and its biological functions. Nat. Rev. Mol. Cell Biol. 2020, 22, 96–118.
Iyer, M.K.; Niknafs, Y.S.; Malik, R.; Singhal, U.; Sahu, A.; Hosono, Y.; Barrette, T.R.; Prensner, J.R.; Evans, J.R.; Zhao, S.; et al. The landscape of long noncoding RNAs in the human transcriptome. Nat. Genet. 2015, 47, 199–208.
Yu, T.; Shan, T.D.; Li, J.Y.; Huang, C.Z.; Wang, S.Y.; Ouyang, H.; Lu, X.J.; Xu, J.H.; Zhong, W.; Chen, Q.K. Knockdown of linc-UFC1 suppresses proliferation and induces apoptosis of colorectal cancer. Cell Death Dis. 2016, 7, e2228.
Beckedorff, F.C.; Amaral, M.S.; Deocesano-Pereira, C.; Verjovski-Almeida, S. Long non-coding RNAs and their implications in cancer epigenetics. Biosci. Rep. 2013, 33, 54.
Kuang, M.; Yang, M.; Li, L.; Li, C.; Wang, G. UFM1-Specific Ligase 1 Ligating Enzyme 1 Mediates Milk Protein and Fat Synthesis-Related Gene Expression via the JNK Signaling Pathway in Mouse Mammary Epithelial Cells. Oxid. Med. Cell Longev. 2020, 2020, 4045674.
Lin, J.X.; Yoon, C.; Li, P.; Ryeom, S.W.; Cho, S.J.; Zheng, C.H.; Xie, J.W.; Wang, J.B.; Lu, J.; Chen, Q.Y.; et al. CDK5RAP3 as tumour suppressor negatively regulates self-renewal and invasion and is regulated by ERK1/2 signalling in human gastric cancer. Br. J. Cancer 2020, 123, 1131–1144.
Chen, Q.Y.; Liu, L.C.; Wang, J.B.; Xie, J.W.; Lin, J.X.; Lu, J.; Cao, L.L.; Lin, M.; Tu, R.H.; Huang, C.M.; et al. CDK5RAP3 Inhibits the Translocation of MCM6 to Influence the Prognosis in Gastric Cancer. J. Cancer 2019, 10, 4488–4498.
Lin, J.X.; Xie, X.S.; Weng, X.F.; Zheng, C.H.; Xie, J.W.; Wang, J.B.; Lu, J.; Chen, Q.Y.; Cao, L.L.; Lin, M.; et al. Low expression of CDK5RAP3 and DDRGK1 indicates a poor prognosis in patients with gastric cancer. World J. Gastroenterol. 2018, 24, 3898–3907.
Yang, G.; Wang, Y.; Chen, Y.; Huang, R. UFL1 attenuates IL-1beta-induced inflammatory response in human osteoarthritis chondrocytes. Int. Immunopharmacol. 2020, 81, 106278.
Harper, J.W.; Elledge, S.J. The DNA damage response: Ten years after. Mol. Cell 2007, 28, 739–745.
Lamarche, B.J.; Orazio, N.I.; Weitzman, M.D. The MRN complex in double-strand break repair and telomere maintenance. FEBS Lett. 2010, 584, 3682–3695.
Qin, B.; Yu, J.; Nowsheen, S.; Zhao, F.; Wang, L.; Lou, Z. STK38 promotes ATM activation by acting as a reader of histone H4 ufmylation. Sci. Adv. 2020, 6, eaax8214.
Dai, C.; Gu, W. p53 post-translational modification: Deregulated in tumorigenesis. Trends Mol. Med. 2010, 16, 528–536.
Fang, Z.; Pan, Z. Essential Role of Ubiquitin-Fold Modifier 1 Conjugation in DNA Damage Response. DNA Cell Biol. 2019, 38, 1030–1039.
Let us know your experience and what we could improve.
Report an Issue
Is something wrong? Please let us know!
Other Feedback
Other feedback you would like to report.
Did you find what you were looking for?
Love
Like
Neutral
Dislike
Hate
0/500
Email
Do you agree to share your valuable feedback publicly on Encyclopedia’s homepage?
Webpage
Upload a screenshot (Max file size 2MB)
Submit
Back
Close
Quick Survey
Encyclopedia MDPI is conducting a targeted survey to identify the specific barriers hindering efficient
research. We invite you to spend 3 minutes defining the priorities for our next generation of structured
knowledge tools.