UFM1: Comparison
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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
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References

  1. Wei, Y.; Xu, X. UFMylation: A Unique & Fashionable Modification for Life. Genom. Proteom. Bioinform. 2016, 14, 140–146.
  2. 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.
  3. 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.
  4. 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.
  5. 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.
  6. 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.
  7. 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.
  8. 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.
  9. 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.
  10. 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.
  11. 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.
  12. 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.
  13. 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.
  14. 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.
  15. 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.
  16. 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.
  17. Daniel, J.; Liebau, E. The ufm1 cascade. Cells 2014, 3, 627–638.
  18. 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.
  19. 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.
  20. 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.
  21. 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.
  22. 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.
  23. 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.
  24. Scheel, H.; Hofmann, K. Prediction of a common structural scaffold for proteasome lid, COP9-signalosome and eIF3 complexes. BMC Bioinform. 2005, 6, 71.
  25. 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.
  26. Qin, B.; Yu, J.; Nowsheen, S.; Wang, M.; Tu, X.; Liu, T.; Li, H.; Wang, L.; Lou, Z. UFL1 promotes histone H4 ufmylation and ATM activation. Nat. Commun. 2019, 10, 1242.
  27. Wang, Z.; Gong, Y.; Peng, B.; Shi, R.; Fan, D.; Zhao, H.; Zhu, M.; Zhang, H.; Lou, Z.; Zhou, J.; et al. MRE11 UFMylation promotes ATM activation. Nucleic Acids Res. 2019, 47, 4124–4135.
  28. 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.
  29. 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.
  30. 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.
  31. 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.
  32. 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.
  33. 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.
  34. 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.
  35. 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.
  36. 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.
  37. 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.
  38. 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.
  39. 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.
  40. Gerakis, Y.; Quintero, M.; Li, H.; Hetz, C. The UFMylation System in Proteostasis and Beyond. Trends Cell Biol. 2019, 29, 974–986.
  41. Cai, Y.; Singh, N.; Li, H. Essential role of Ufm1 conjugation in the hematopoietic system. Exp. Hematol. 2016, 44, 442–446.
  42. 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.
  43. 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.
  44. 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.
  45. 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.
  46. 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.
  47. 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.
  48. 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.
  49. 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.
  50. 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.
  51. 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.
  52. 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.
  53. 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.
  54. Bruce, A.E.E.; Heisenberg, C.P. Mechanisms of zebrafish epiboly: A current view. Curr. Top. Dev. Biol. 2020, 136, 319–341.
  55. Sharma, S.; Sicinski, P. A kinase of many talents: Non-neuronal functions of CDK5 in development and disease. Open Biol. 2020, 10, 190287.
  56. 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.
  57. Ching, Y.P.; Qi, Z.; Wang, J.H. Cloning of three novel neuronal Cdk5 activator binding proteins. Gene 2000, 242, 285–294.
  58. 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.
  59. Hetz, C. The unfolded protein response: Controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 2012, 13, 89–102.
  60. 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.
  61. Chen, Y.; Zhang, Y.; Yin, Y.; Gao, G.; Li, S.; Jiang, Y.; Gu, X.; Luo, J. SPD—A web-based secreted protein database. Nucleic Acids Res. 2005, 33, D169–D173.
  62. Rashid, H.O.; Yadav, R.K.; Kim, H.R.; Chae, H.J. ER stress: Autophagy induction, inhibition and selection. Autophagy 2015, 11, 1956–1977.
  63. 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.
  64. 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.
  65. 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.
  66. Bagola, K.; Mehnert, M.; Jarosch, E.; Sommer, T. Protein dislocation from the ER. Biochim. Biophys. Acta 2011, 1808, 925–936.
  67. 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.
  68. 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.
  69. 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.
  70. Dikic, I.; Elazar, Z. Mechanism and medical implications of mammalian autophagy. Nat. Rev. Mol. Cell Biol. 2018, 19, 349–364.
  71. 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.
  72. Li, J.; Yue, G.; Ma, W.; Zhang, A.; Zou, J.; Cai, Y.; Tang, X.; Wang, J.; Liu, J.; Li, H.; et al. Ufm1-Specific Ligase Ufl1 Regulates Endoplasmic Reticulum Homeostasis and Protects Against Heart Failure. Circ. Heart Fail. 2018, 11, e004917.
  73. 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.
  74. Johansen, T.; Lamark, T. Selective Autophagy: ATG8 Family Proteins, LIR Motifs and Cargo Receptors. J. Mol. Biol. 2020, 432, 80–103.
  75. Stolz, A.; Ernst, A.; Dikic, I. Cargo recognition and trafficking in selective autophagy. Nat. Cell Biol. 2014, 16, 495–501.
  76. 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.
  77. Strzyz, P. Foundations of ER-phagy regulation. Nat. Rev. Mol. Cell Biol. 2020, 21, 251.
  78. Jarc, E.; Petan, T. Lipid Droplets and the Management of Cellular Stress. Yale J. Biol. Med. 2019, 92, 435–452.
  79. 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.
  80. 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.
  81. 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.
  82. 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.
  83. 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.
  84. Li, Y.Y.; Zhang, G.Y.; He, J.P.; Zhang, D.D.; Kong, X.X.; Yuan, H.M.; Chen, F.L. Ufm1 inhibits LPS-induced endothelial cell inflammatory responses through the NF-kappaB signaling pathway. Int. J. Mol. Med. 2017, 39, 1119–1126.
  85. 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.
  86. 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.
  87. 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.
  88. 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.
  89. Yang, G.; Wang, Y.; Chen, Y.; Huang, R. UFL1 attenuates IL-1beta-induced inflammatory response in human osteoarthritis chondrocytes. Int. Immunopharmacol. 2020, 81, 106278.
  90. Harper, J.W.; Elledge, S.J. The DNA damage response: Ten years after. Mol. Cell 2007, 28, 739–745.
  91. 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.
  92. 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.
  93. Dai, C.; Gu, W. p53 post-translational modification: Deregulated in tumorigenesis. Trends Mol. Med. 2010, 16, 528–536.
  94. Fang, Z.; Pan, Z. Essential Role of Ubiquitin-Fold Modifier 1 Conjugation in DNA Damage Response. DNA Cell Biol. 2019, 38, 1030–1039.
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