Emerging Role of Deubiquitinating Enzymes (DUBs) in Melanoma Pathogenesis
Abstract
:Simple Summary
Abstract
1. Introduction
1.1. Melanoma
1.2. The Ubiquitin Pathway
2. Deubiquitinating Enzymes in Melanoma
2.1. Ubiquitin-Specific Proteases (USPs)
2.1.1. USP4
2.1.2. USP5
2.1.3. USP7
2.1.4. USP9X
2.1.5. USP13
2.1.6. USP14
2.1.7. USP15
2.1.8. USP22
2.1.9. USP28
2.1.10. CYLD
2.2. JAB1/MPN/MOV34 Metalloenzymes (JAMMs)
2.2.1. MYSM1
2.2.2. PSMD14
3. Conclusions and Perspectives
Author Contributions
Funding
Conflicts of Interest
References
- Miller, A.J.; Mihm, M.C., Jr. Melanoma. N. Engl. J. Med. 2006, 355, 51–65. [Google Scholar] [CrossRef] [PubMed]
- Shain, A.H.; Bastian, B.C. From melanocytes to melanomas. Nat. Rev. Cancer 2016, 16, 345–358. [Google Scholar] [CrossRef] [PubMed]
- Maxwell, R.; Garzon-Muvdi, T.; Lipson, E.J.; Sharfman, W.H.; Bettegowda, C.; Redmond, K.J.; Kleinberg, L.R.; Ye, X.; Lim, M. BRAF-V600 mutational status affects recurrence patterns of melanoma brain metastasis. Int. J. Cancer 2017, 140, 2716–2727. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Achrol, A.S.; Rennert, R.C.; Anders, C.; Soffietti, R.; Ahluwalia, M.S.; Nayak, L.; Peters, S.; Arvold, N.D.; Harsh, G.R.; Steeg, P.S.; et al. Brain metastases. Nat. Rev. Dis. Primers 2019, 5, 5. [Google Scholar] [CrossRef]
- Pierard-Franchimont, C.; Hermanns-Le, T.; Delvenne, P.; Pierard, G.E. Dormancy of growth-stunted malignant melanoma: Sustainable and smoldering patterns. Oncol. Rev. 2014, 8, 252. [Google Scholar] [CrossRef] [Green Version]
- Balch, C.M.; Gershenwald, J.E.; Soong, S.J.; Thompson, J.F.; Atkins, M.B.; Byrd, D.R.; Buzaid, A.C.; Cochran, A.J.; Coit, D.G.; Ding, S.; et al. Final version of 2009 AJCC melanoma staging and classification. J. Clin. Oncol. 2009, 27, 6199–6206. [Google Scholar] [CrossRef] [Green Version]
- Hodis, E.; Watson, I.R.; Kryukov, G.V.; Arold, S.T.; Imielinski, M.; Theurillat, J.P.; Nickerson, E.; Auclair, D.; Li, L.; Place, C.; et al. A landscape of driver mutations in melanoma. Cell 2012, 150, 251–263. [Google Scholar] [CrossRef] [Green Version]
- McArthur, G.A.; Ribas, A. Targeting oncogenic drivers and the immune system in melanoma. J. Clin. Oncol. 2013, 31, 499–506. [Google Scholar] [CrossRef]
- Stadler, S.; Weina, K.; Gebhardt, C.; Utikal, J. New therapeutic options for advanced non-resectable malignant melanoma. Adv. Med. Sci. 2015, 60, 83–88. [Google Scholar] [CrossRef]
- Nazarian, R.; Shi, H.; Wang, Q.; Kong, X.; Koya, R.C.; Lee, H.; Chen, Z.; Lee, M.K.; Attar, N.; Sazegar, H.; et al. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 2010, 468, 973–977. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Leite de Oliveira, R.; Huijberts, S.; Bosdriesz, E.; Pencheva, N.; Brunen, D.; Bosma, A.; Song, J.Y.; Zevenhoven, J.; Los-de Vries, G.T.; et al. An Acquired Vulnerability of Drug-Resistant Melanoma with Therapeutic Potential. Cell 2018, 173, 1413–1425.e14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Poulikakos, P.I.; Persaud, Y.; Janakiraman, M.; Kong, X.; Ng, C.; Moriceau, G.; Shi, H.; Atefi, M.; Titz, B.; Gabay, M.T.; et al. RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature 2011, 480, 387–390. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moriceau, G.; Hugo, W.; Hong, A.; Shi, H.; Kong, X.; Yu, C.C.; Koya, R.C.; Samatar, A.A.; Khanlou, N.; Braun, J.; et al. Tunable-combinatorial mechanisms of acquired resistance limit the efficacy of BRAF/MEK cotargeting but result in melanoma drug addiction. Cancer Cell 2015, 27, 240–256. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Su, Y.; Ko, M.E.; Cheng, H.; Zhu, R.; Xue, M.; Wang, J.; Lee, J.W.; Frankiw, L.; Xu, A.; Wong, S.; et al. Multi-omic single-cell snapshots reveal multiple independent trajectories to drug tolerance in a melanoma cell line. Nat. Commun. 2020, 11, 2345. [Google Scholar] [CrossRef] [PubMed]
- Torre, E.A.; Arai, E.; Bayatpour, S.; Jiang, C.L.; Beck, L.E.; Emert, B.L.; Shaffer, S.M.; Mellis, I.A.; Fane, M.E.; Alicea, G.M.; et al. Genetic screening for single-cell variability modulators driving therapy resistance. Nat. Genet. 2021, 53, 76–85. [Google Scholar] [CrossRef]
- Emmons, M.F.; Faiao-Flores, F.; Smalley, K.S.M. The role of phenotypic plasticity in the escape of cancer cells from targeted therapy. Biochem. Pharmacol. 2016, 122, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Oren, Y.; Tsabar, M.; Cuoco, M.S.; Amir-Zilberstein, L.; Cabanos, H.F.; Hutter, J.C.; Hu, B.; Thakore, P.I.; Tabaka, M.; Fulco, C.P.; et al. Cycling cancer persister cells arise from lineages with distinct programs. Nature 2021, 596, 576–582. [Google Scholar] [CrossRef]
- Fallahi-Sichani, M.; Becker, V.; Izar, B.; Baker, G.J.; Lin, J.R.; Boswell, S.A.; Shah, P.; Rotem, A.; Garraway, L.A.; Sorger, P.K. Adaptive resistance of melanoma cells to RAF inhibition via reversible induction of a slowly dividing de-differentiated state. Mol. Syst. Biol. 2017, 13, 905. [Google Scholar] [CrossRef]
- Hugo, W.; Shi, H.; Sun, L.; Piva, M.; Song, C.; Kong, X.; Moriceau, G.; Hong, A.; Dahlman, K.B.; Johnson, D.B.; et al. Non-genomic and Immune Evolution of Melanoma Acquiring MAPKi Resistance. Cell 2015, 162, 1271–1285. [Google Scholar] [CrossRef] [Green Version]
- Ohanna, M.; Cerezo, M.; Nottet, N.; Bille, K.; Didier, R.; Beranger, G.; Mograbi, B.; Rocchi, S.; Yvan-Charvet, L.; Ballotti, R.; et al. Pivotal role of NAMPT in the switch of melanoma cells toward an invasive and drug-resistant phenotype. Genes Dev. 2018, 32, 448–461. [Google Scholar] [CrossRef]
- Ratnikov, B.I.; Scott, D.A.; Osterman, A.L.; Smith, J.W.; Ronai, Z.A. Metabolic rewiring in melanoma. Oncogene 2017, 36, 147–157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luke, J.J.; Flaherty, K.T.; Ribas, A.; Long, G.V. Targeted agents and immunotherapies: Optimizing outcomes in melanoma. Nat. Rev. Clin. Oncol. 2017, 14, 463–482. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schadendorf, D.; Hodi, F.S.; Robert, C.; Weber, J.S.; Margolin, K.; Hamid, O.; Patt, D.; Chen, T.T.; Berman, D.M.; Wolchok, J.D. Pooled Analysis of Long-Term Survival Data from Phase II and Phase III Trials of Ipilimumab in Unresectable or Metastatic Melanoma. J. Clin. Oncol. 2015, 33, 1889–1894. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weber, J.S.; D’Angelo, S.P.; Minor, D.; Hodi, F.S.; Gutzmer, R.; Neyns, B.; Hoeller, C.; Khushalani, N.I.; Miller, W.H., Jr.; Lao, C.D.; et al. Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): A randomised, controlled, open-label, phase 3 trial. Lancet Oncol. 2015, 16, 375–384. [Google Scholar] [CrossRef]
- Wan, M.T.; Ming, M.E. Nivolumab versus ipilimumab in the treatment of advanced melanoma: A critical appraisal: ORIGINAL ARTICLE: Wolchok, J.D.; Chiarion-Sileni, V.; Gonzalez, R.; et al. Overall survival with combined nivolumab and ipilimumab in advanced melanoma. N. Engl. J. Med. 2017, 377, 1345–1356. [Google Scholar] [CrossRef]
- Larkin, J.; Chiarion-Sileni, V.; Gonzalez, R.; Grob, J.J.; Cowey, C.L.; Lao, C.D.; Schadendorf, D.; Dummer, R.; Smylie, M.; Rutkowski, P.; et al. Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma. N. Engl. J. Med. 2015, 373, 23–34. [Google Scholar] [CrossRef] [Green Version]
- Fares, C.M.; Van Allen, E.M.; Drake, C.G.; Allison, J.P.; Hu-Lieskovan, S. Mechanisms of Resistance to Immune Checkpoint Blockade: Why Does Checkpoint Inhibitor Immunotherapy Not Work for All Patients? Am. Soc. Clin. Oncol. Educ. Book 2019, 39, 147–164. [Google Scholar] [CrossRef]
- Ribas, A.; Wolchok, J.D. Cancer immunotherapy using checkpoint blockade. Science 2018, 359, 1350–1355. [Google Scholar] [CrossRef] [Green Version]
- Lim, S.; Phillips, J.B.; Madeira da Silva, L.; Zhou, M.; Fodstad, O.; Owen, L.B.; Tan, M. Interplay between Immune Checkpoint Proteins and Cellular Metabolism. Cancer Res. 2017, 77, 1245–1249. [Google Scholar] [CrossRef] [Green Version]
- Komander, D.; Rape, M. The ubiquitin code. Annu. Rev. Biochem. 2012, 81, 203–229. [Google Scholar] [CrossRef] [Green Version]
- Hershko, A.; Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67, 425–479. [Google Scholar] [CrossRef] [PubMed]
- McClellan, A.J.; Laugesen, S.H.; Ellgaard, L. Cellular functions and molecular mechanisms of non-lysine ubiquitination. Open Biol. 2019, 9, 190147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hicke, L. Protein regulation by monoubiquitin. Nat. Rev. Mol. Cell Biol. 2001, 2, 195–201. [Google Scholar] [CrossRef] [PubMed]
- Hoeller, D.; Dikic, I. Regulation of ubiquitin receptors by coupled monoubiquitination. Subcell. Biochem. 2010, 54, 31–40. [Google Scholar] [CrossRef] [PubMed]
- Mozuraitiene, J.; Gudleviciene, Z.; Vincerzevskiene, I.; Laurinaviciene, A.; Pamedys, J. Expression levels of FBXW7 and MDM2 E3 ubiquitin ligases and their c-Myc and p53 substrates in patients with dysplastic nevi or melanoma. Oncol. Lett. 2021, 21, 37. [Google Scholar] [CrossRef]
- Nijman, S.M.; Luna-Vargas, M.P.; Velds, A.; Brummelkamp, T.R.; Dirac, A.M.; Sixma, T.K.; Bernards, R. A genomic and functional inventory of deubiquitinating enzymes. Cell 2005, 123, 773–786. [Google Scholar] [CrossRef] [Green Version]
- Fraile, J.M.; Quesada, V.; Rodriguez, D.; Freije, J.M.; Lopez-Otin, C. Deubiquitinases in cancer: New functions and therapeutic options. Oncogene 2012, 31, 2373–2388. [Google Scholar] [CrossRef] [Green Version]
- Ge, Z.; Leighton, J.S.; Wang, Y.; Peng, X.; Chen, Z.; Chen, H.; Sun, Y.; Yao, F.; Li, J.; Zhang, H.; et al. Integrated Genomic Analysis of the Ubiquitin Pathway across Cancer Types. Cell Rep. 2018, 23, 213–226.e213. [Google Scholar] [CrossRef] [Green Version]
- Guo, W.; Ma, J.; Pei, T.; Zhao, T.; Guo, S.; Yi, X.; Liu, Y.; Wang, S.; Zhu, G.; Jian, Z.; et al. Up-regulated deubiquitinase USP4 plays an oncogenic role in melanoma. J. Cell Mol. Med. 2018, 22, 2944–2954. [Google Scholar] [CrossRef]
- Zhang, X.; Berger, F.G.; Yang, J.; Lu, X. USP4 inhibits p53 through deubiquitinating and stabilizing ARF-BP1. EMBO J. 2011, 30, 2177–2189. [Google Scholar] [CrossRef]
- Liu, H.; Zhang, H.; Wang, X.; Tian, Q.; Hu, Z.; Peng, C.; Jiang, P.; Wang, T.; Guo, W.; Chen, Y.; et al. The Deubiquitylating Enzyme USP4 Cooperates with CtIP in DNA Double-Strand Break End Resection. Cell Rep. 2015, 13, 93–107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, L.; Zhou, F.; Drabsch, Y.; Gao, R.; Snaar-Jagalska, B.E.; Mickanin, C.; Huang, H.; Sheppard, K.A.; Porter, J.A.; Lu, C.X.; et al. USP4 is regulated by AKT phosphorylation and directly deubiquitylates TGF-beta type I receptor. Nat. Cell Biol. 2012, 14, 717–726. [Google Scholar] [CrossRef] [PubMed]
- Potu, H.; Peterson, L.F.; Pal, A.; Verhaegen, M.; Cao, J.; Talpaz, M.; Donato, N.J. Usp5 links suppression of p53 and FAS levels in melanoma to the BRAF pathway. Oncotarget 2014, 5, 5559–5569. [Google Scholar] [CrossRef] [Green Version]
- Meng, J.; Ai, X.; Lei, Y.; Zhong, W.; Qian, B.; Qiao, K.; Wang, X.; Zhou, B.; Wang, H.; Huai, L.; et al. USP5 promotes epithelial-mesenchymal transition by stabilizing SLUG in hepatocellular carcinoma. Theranostics 2019, 9, 573–587. [Google Scholar] [CrossRef] [PubMed]
- Kapuria, V.; Peterson, L.F.; Fang, D.; Bornmann, W.G.; Talpaz, M.; Donato, N.J. Deubiquitinase inhibition by small-molecule WP1130 triggers aggresome formation and tumor cell apoptosis. Cancer Res. 2010, 70, 9265–9276. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pal, A.; Dziubinski, M.; Di Magliano, M.P.; Simeone, D.M.; Owens, S.; Thomas, D.; Peterson, L.; Potu, H.; Talpaz, M.; Donato, N.J. Usp9x Promotes Survival in Human Pancreatic Cancer and Its Inhibition Suppresses Pancreatic Ductal Adenocarcinoma In Vivo Tumor Growth. Neoplasia 2018, 20, 152–164. [Google Scholar] [CrossRef]
- Li, M.; Chen, D.; Shiloh, A.; Luo, J.; Nikolaev, A.Y.; Qin, J.; Gu, W. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 2002, 416, 648–653. [Google Scholar] [CrossRef]
- Rai, K.; Akdemir, K.C.; Kwong, L.N.; Fiziev, P.; Wu, C.J.; Keung, E.Z.; Sharma, S.; Samant, N.S.; Williams, M.; Axelrad, J.B.; et al. Dual Roles of RNF2 in Melanoma Progression. Cancer Discov. 2015, 5, 1314–1327. [Google Scholar] [CrossRef] [Green Version]
- Su, D.; Wang, W.; Hou, Y.; Wang, L.; Yi, X.; Cao, C.; Wang, Y.; Gao, H.; Wang, Y.; Yang, C.; et al. Bimodal regulation of the PRC2 complex by USP7 underlies tumorigenesis. Nucleic Acids Res. 2021, 49, 4421–4440. [Google Scholar] [CrossRef]
- Gao, L.; Zhu, D.; Wang, Q.; Bao, Z.; Yin, S.; Qiang, H.; Wieland, H.; Zhang, J.; Teichmann, A.; Jia, J. Proteome Analysis of USP7 Substrates Revealed Its Role in Melanoma through PI3K/Akt/FOXO and AMPK Pathways. Front. Oncol. 2021, 11, 650165. [Google Scholar] [CrossRef]
- Xiang, M.; Liang, L.; Kuang, X.; Xie, Z.; Liu, J.; Zhao, S.; Su, J.; Chen, X.; Liu, H. Pharmacological inhibition of USP7 suppresses growth and metastasis of melanoma cells in vitro and in vivo. J. Cell Mol. Med. 2021, 25, 9228–9240. [Google Scholar] [CrossRef] [PubMed]
- Potu, H.; Kandarpa, M.; Peterson, L.F.; Durham, A.; Donato, N.J.; Talpaz, M. Downregulation of SOX2 by inhibition of Usp9X induces apoptosis in melanoma. Oncotarget 2021, 12, 160–172. [Google Scholar] [CrossRef] [PubMed]
- Potu, H.; Peterson, L.F.; Kandarpa, M.; Pal, A.; Sun, H.; Durham, A.; Harms, P.W.; Hollenhorst, P.C.; Eskiocak, U.; Talpaz, M.; et al. Usp9x regulates Ets-1 ubiquitination and stability to control NRAS expression and tumorigenicity in melanoma. Nat. Commun. 2017, 8, 14449. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, X.; Zhang, X.; Cai, H.; Yang, W.; Lei, H.; Xu, H.; Wang, W.; Zhu, Q.; Kang, J.; Yin, T.; et al. Targeting USP9x/SOX2 axis contributes to the anti-osteosarcoma effect of neogambogic acid. Cancer Lett. 2020, 469, 277–286. [Google Scholar] [CrossRef]
- Zhao, X.; Fiske, B.; Kawakami, A.; Li, J.; Fisher, D.E. Regulation of MITF stability by the USP13 deubiquitinase. Nat. Commun. 2011, 2, 414. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marshall, R.S.; Vierstra, R.D. Dynamic Regulation of the 26S Proteasome: From Synthesis to Degradation. Front. Mol. Biosci. 2019, 6, 40. [Google Scholar] [CrossRef] [PubMed]
- Koulich, E.; Li, X.; DeMartino, G.N. Relative structural and functional roles of multiple deubiquitylating proteins associated with mammalian 26S proteasome. Mol. Biol. Cell 2008, 19, 1072–1082. [Google Scholar] [CrossRef] [Green Version]
- Kim, E.; Park, S.; Lee, J.H.; Mun, J.Y.; Choi, W.H.; Yun, Y.; Lee, J.; Kim, J.H.; Kang, M.J.; Lee, M.J. Dual Function of USP14 Deubiquitinase in Cellular Proteasomal Activity and Autophagic Flux. Cell Rep. 2018, 24, 732–743. [Google Scholar] [CrossRef] [Green Version]
- Didier, R.; Mallavialle, A.; Ben Jouira, R.; Domdom, M.A.; Tichet, M.; Auberger, P.; Luciano, F.; Ohanna, M.; Tartare-Deckert, S.; Deckert, M. Targeting the Proteasome-Associated Deubiquitinating Enzyme USP14 Impairs Melanoma Cell Survival and Overcomes Resistance to MAPK-Targeting Therapies. Mol. Cancer Ther. 2018, 17, 1416–1429. [Google Scholar] [CrossRef] [Green Version]
- Chen, X.; Wu, Q.; Tan, L.; Porter, D.; Jager, M.J.; Emery, C.; Bastian, B.C. Combined PKC and MEK inhibition in uveal melanoma with GNAQ and GNA11 mutations. Oncogene 2014, 33, 4724–4734. [Google Scholar] [CrossRef] [Green Version]
- Zou, Q.; Jin, J.; Hu, H.; Li, H.S.; Romano, S.; Xiao, Y.; Nakaya, M.; Zhou, X.; Cheng, X.; Yang, P.; et al. USP15 stabilizes MDM2 to mediate cancer-cell survival and inhibit antitumor T cell responses. Nat. Immunol. 2014, 15, 562–570. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, L.L.; Smith, M.D.; Lv, L.; Nakagawa, T.; Li, Z.; Sun, S.C.; Brown, N.G.; Xiong, Y.; Xu, Y.P. USP15 suppresses tumor immunity via deubiquitylation and inactivation of TET2. Sci. Adv. 2020, 6, eabc9730. [Google Scholar] [CrossRef] [PubMed]
- Eichhorn, P.J.; Rodon, L.; Gonzalez-Junca, A.; Dirac, A.; Gili, M.; Martinez-Saez, E.; Aura, C.; Barba, I.; Peg, V.; Prat, A.; et al. USP15 stabilizes TGF-beta receptor I and promotes oncogenesis through the activation of TGF-beta signaling in glioblastoma. Nat. Med. 2012, 18, 429–435. [Google Scholar] [CrossRef] [PubMed]
- Schweitzer, K.; Bozko, P.M.; Dubiel, W.; Naumann, M. CSN controls NF-kappaB by deubiquitinylation of IkappaBalpha. EMBO J. 2007, 26, 1532–1541. [Google Scholar] [CrossRef] [PubMed]
- Pauli, E.K.; Chan, Y.K.; Davis, M.E.; Gableske, S.; Wang, M.K.; Feister, K.F.; Gack, M.U. The ubiquitin-specific protease USP15 promotes RIG-I-mediated antiviral signaling by deubiquitylating TRIM25. Sci. Signal. 2014, 7, ra3. [Google Scholar] [CrossRef] [Green Version]
- Luise, C.; Capra, M.; Donzelli, M.; Mazzarol, G.; Jodice, M.G.; Nuciforo, P.; Viale, G.; Di Fiore, P.P.; Confalonieri, S. An atlas of altered expression of deubiquitinating enzymes in human cancer. PLoS ONE 2011, 6, e15891. [Google Scholar] [CrossRef]
- Wei, Y.; Jiang, Z.; Lu, J. USP22 promotes melanoma and BRAF inhibitor resistance via YAP stabilization. Oncol. Lett. 2021, 21, 394. [Google Scholar] [CrossRef]
- Li, M.; Xu, Y.; Liang, J.; Lin, H.; Qi, X.; Li, F.; Han, P.; Gao, Y.; Yang, X. USP22 deficiency in melanoma mediates resistance to T cells through IFNgamma-JAK1-STAT1 signal axis. Mol. Ther. 2021, 29, 2108–2120. [Google Scholar] [CrossRef]
- Wang, Y.; Sun, Q.; Mu, N.; Sun, X.; Wang, Y.; Fan, S.; Su, L.; Liu, X. The deubiquitinase USP22 regulates PD-L1 degradation in human cancer cells. Cell Commun. Signal. 2020, 18, 112. [Google Scholar] [CrossRef]
- Huang, X.; Zhang, Q.; Lou, Y.; Wang, J.; Zhao, X.; Wang, L.; Zhang, X.; Li, S.; Zhao, Y.; Chen, Q.; et al. USP22 Deubiquitinates CD274 to Suppress Anticancer Immunity. Cancer Immunol. Res. 2019, 7, 1580–1590. [Google Scholar] [CrossRef] [Green Version]
- Jeusset, L.M.; McManus, K.J. Ubiquitin Specific Peptidase 22 Regulates Histone H2B Mono-Ubiquitination and Exhibits Both Oncogenic and Tumor Suppressor Roles in Cancer. Cancers 2017, 9, 167. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Atanassov, B.S.; Evrard, Y.A.; Multani, A.S.; Zhang, Z.; Tora, L.; Devys, D.; Chang, S.; Dent, S.Y. Gcn5 and SAGA regulate shelterin protein turnover and telomere maintenance. Mol. Cell 2009, 35, 352–364. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xiao, H.; Tian, Y.; Yang, Y.; Hu, F.; Xie, X.; Mei, J.; Ding, F. USP22 acts as an oncogene by regulating the stability of cyclooxygenase-2 in non-small cell lung cancer. Biochem. Biophys. Res. Commun. 2015, 460, 703–708. [Google Scholar] [CrossRef] [PubMed]
- Lin, Z.; Tan, C.; Qiu, Q.; Kong, S.; Yang, H.; Zhao, F.; Liu, Z.; Li, J.; Kong, Q.; Gao, B.; et al. Ubiquitin-specific protease 22 is a deubiquitinase of CCNB1. Cell Discov. 2015, 1, 15028. [Google Scholar] [CrossRef] [PubMed]
- Ling, S.; Li, J.; Shan, Q.; Dai, H.; Lu, D.; Wen, X.; Song, P.; Xie, H.; Zhou, L.; Liu, J.; et al. USP22 mediates the multidrug resistance of hepatocellular carcinoma via the SIRT1/AKT/MRP1 signaling pathway. Mol. Oncol. 2017, 11, 682–695. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ohanna, M.; Bonet, C.; Bille, K.; Allegra, M.; Davidson, I.; Bahadoran, P.; Lacour, J.P.; Ballotti, R.; Bertolotto, C. SIRT1 promotes proliferation and inhibits the senescence-like phenotype in human melanoma cells. Oncotarget 2014, 5, 2085–2095. [Google Scholar] [CrossRef] [Green Version]
- Wang, Z.; Song, Q.; Xue, J.; Zhao, Y.; Qin, S. Ubiquitin-specific protease 28 is overexpressed in human glioblastomas and contributes to glioma tumorigenicity by regulating MYC expression. Exp. Biol. Med. 2016, 241, 255–264. [Google Scholar] [CrossRef] [Green Version]
- Li, Z.H.; Yu, Y.; Du, C.; Fu, H.; Wang, J.; Tian, Y. RNA interference-mediated USP22 gene silencing promotes human brain glioma apoptosis and induces cell cycle arrest. Oncol. Lett. 2013, 5, 1290–1294. [Google Scholar] [CrossRef] [Green Version]
- Popov, N.; Wanzel, M.; Madiredjo, M.; Zhang, D.; Beijersbergen, R.; Bernards, R.; Moll, R.; Elledge, S.J.; Eilers, M. The ubiquitin-specific protease USP28 is required for MYC stability. Nat. Cell Biol. 2007, 9, 765–774. [Google Scholar] [CrossRef]
- Saei, A.; Palafox, M.; Benoukraf, T.; Kumari, N.; Jaynes, P.W.; Iyengar, P.V.; Munoz-Couselo, E.; Nuciforo, P.; Cortes, J.; Notzel, C.; et al. Loss of USP28-mediated BRAF degradation drives resistance to RAF cancer therapies. J. Exp. Med. 2018, 215, 1913–1928. [Google Scholar] [CrossRef] [Green Version]
- Zhang, D.; Zaugg, K.; Mak, T.W.; Elledge, S.J. A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell 2006, 126, 529–542. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Richter, K.; Paakkola, T.; Mennerich, D.; Kubaichuk, K.; Konzack, A.; Ali-Kippari, H.; Kozlova, N.; Koivunen, P.; Haapasaari, K.M.; Jukkola-Vuorinen, A.; et al. USP28 Deficiency Promotes Breast and Liver Carcinogenesis as well as Tumor Angiogenesis in a HIF-independent Manner. Mol. Cancer Res. 2018, 16, 1000–1012. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chipumuro, E.; Henriksen, M.A. The ubiquitin hydrolase USP22 contributes to 3′-end processing of JAK-STAT-inducible genes. FASEB J. 2012, 26, 842–854. [Google Scholar] [CrossRef] [PubMed]
- Meitinger, F.; Anzola, J.V.; Kaulich, M.; Richardson, A.; Stender, J.D.; Benner, C.; Glass, C.K.; Dowdy, S.F.; Desai, A.; Shiau, A.K.; et al. 53BP1 and USP28 mediate p53 activation and G1 arrest after centrosome loss or extended mitotic duration. J. Cell Biol. 2016, 214, 155–166. [Google Scholar] [CrossRef] [PubMed]
- Massoumi, R.; Kuphal, S.; Hellerbrand, C.; Haas, B.; Wild, P.; Spruss, T.; Pfeifer, A.; Fassler, R.; Bosserhoff, A.K. Down-regulation of CYLD expression by Snail promotes tumor progression in malignant melanoma. J. Exp. Med. 2009, 206, 221–232. [Google Scholar] [CrossRef] [Green Version]
- La, T.; Jin, L.; Liu, X.Y.; Song, Z.H.; Farrelly, M.; Feng, Y.C.; Yan, X.G.; Zhang, Y.Y.; Thorne, R.F.; Zhang, X.D.; et al. Cylindromatosis Is Required for Survival of a Subset of Melanoma Cells. Oncol. Res. 2020, 28, 385–398. [Google Scholar] [CrossRef]
- Ke, H.; Augustine, C.K.; Gandham, V.D.; Jin, J.Y.; Tyler, D.S.; Akiyama, S.K.; Hall, R.P.; Zhang, J.Y. CYLD inhibits melanoma growth and progression through suppression of the JNK/AP-1 and beta1-integrin signaling pathways. J. Investig. Dermatol. 2013, 133, 221–229. [Google Scholar] [CrossRef] [Green Version]
- de Jel, M.M.; Schott, M.; Lamm, S.; Neuhuber, W.; Kuphal, S.; Bosserhoff, A.K. Loss of CYLD accelerates melanoma development and progression in the Tg(Grm1) melanoma mouse model. Oncogenesis 2019, 8, 56. [Google Scholar] [CrossRef] [Green Version]
- Liu, X.Y.; Lai, F.; Yan, X.G.; Jiang, C.C.; Guo, S.T.; Wang, C.Y.; Croft, A.; Tseng, H.Y.; Wilmott, J.S.; Scolyer, R.A.; et al. RIP1 Kinase Is an Oncogenic Driver in Melanoma. Cancer Res. 2015, 75, 1736–1748. [Google Scholar] [CrossRef] [Green Version]
- Zhu, G.; Herlyn, M.; Yang, X. TRIM15 and CYLD regulate ERK activation via lysine-63-linked polyubiquitination. Nat. Cell Biol. 2021, 23, 978–991. [Google Scholar] [CrossRef]
- Zhu, P.; Zhou, W.; Wang, J.; Puc, J.; Ohgi, K.A.; Erdjument-Bromage, H.; Tempst, P.; Glass, C.K.; Rosenfeld, M.G. A histone H2A deubiquitinase complex coordinating histone acetylation and H1 dissociation in transcriptional regulation. Mol. Cell 2007, 27, 609–621. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wilms, C.; Kroeger, C.M.; Hainzl, A.V.; Banik, I.; Bruno, C.; Krikki, I.; Farsam, V.; Wlaschek, M.; Gatzka, M.V. MYSM1/2A-DUB is an epigenetic regulator in human melanoma and contributes to tumor cell growth. Oncotarget 2017, 8, 67287–67299. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kroeger, C.; Roesler, R.; Wiese, S.; Hainzl, A.; Gatzka, M.V. Interaction of Deubiquitinase 2A-DUB/MYSM1 with DNA Repair and Replication Factors. Int. J. Mol. Sci. 2020, 21, 3762. [Google Scholar] [CrossRef]
- Lander, G.C.; Estrin, E.; Matyskiela, M.E.; Bashore, C.; Nogales, E.; Martin, A. Complete subunit architecture of the proteasome regulatory particle. Nature 2012, 482, 186–191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Verma, R.; Aravind, L.; Oania, R.; McDonald, W.H.; Yates, J.R., 3rd; Koonin, E.V.; Deshaies, R.J. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 2002, 298, 611–615. [Google Scholar] [CrossRef]
- Butler, L.R.; Densham, R.M.; Jia, J.; Garvin, A.J.; Stone, H.R.; Shah, V.; Weekes, D.; Festy, F.; Beesley, J.; Morris, J.R. The proteasomal de-ubiquitinating enzyme POH1 promotes the double-strand DNA break response. EMBO J. 2012, 31, 3918–3934. [Google Scholar] [CrossRef]
- Yao, T.; Cohen, R.E. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 2002, 419, 403–407. [Google Scholar] [CrossRef]
- Ben-Aroya, S.; Agmon, N.; Yuen, K.; Kwok, T.; McManus, K.; Kupiec, M.; Hieter, P. Proteasome nuclear activity affects chromosome stability by controlling the turnover of Mms22, a protein important for DNA repair. PLoS Genet. 2010, 6, e1000852. [Google Scholar] [CrossRef] [Green Version]
- Yokoyama, S.; Iwakami, Y.; Hang, Z.; Kin, R.; Zhou, Y.; Yasuta, Y.; Takahashi, A.; Hayakawa, Y.; Sakurai, H. Targeting PSMD14 inhibits melanoma growth through SMAD3 stabilization. Sci. Rep. 2020, 10, 19214. [Google Scholar] [CrossRef]
- Luo, G.; Hu, N.; Xia, X.; Zhou, J.; Ye, C. RPN11 deubiquitinase promotes proliferation and migration of breast cancer cells. Mol. Med. Rep. 2017, 16, 331–338. [Google Scholar] [CrossRef] [Green Version]
- Jing, C.; Duan, Y.; Zhou, M.; Yue, K.; Zhuo, S.; Li, X.; Liu, D.; Ye, B.; Lai, Q.; Li, L.; et al. Blockade of deubiquitinating enzyme PSMD14 overcomes chemoresistance in head and neck squamous cell carcinoma by antagonizing E2F1/Akt/SOX2-mediated stemness. Theranostics 2021, 11, 2655–2669. [Google Scholar] [CrossRef] [PubMed]
- Fenouille, N.; Tichet, M.; Dufies, M.; Pottier, A.; Mogha, A.; Soo, J.K.; Rocchi, S.; Mallavialle, A.; Galibert, M.D.; Khammari, A.; et al. The epithelial-mesenchymal transition (EMT) regulatory factor SLUG (SNAI2) is a downstream target of SPARC and AKT in promoting melanoma cell invasion. PLoS ONE 2012, 7, e40378. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Diazzi, S.; Baeri, A.; Fassy, J.; Lecacheur, M.; Marin-Bejar, O.; Girard, C.A.; Lefevre, L.; Lacoux, C.; Irondelle, M.; Mounier, C.; et al. Blockade of the pro-fibrotic reaction mediated by the miR-143/-145 cluster enhances the responses to targeted therapy in melanoma. EMBO Mol. Med. 2022, 14, e15295. [Google Scholar] [CrossRef] [PubMed]
- Pedri, D.; Karras, P.; Landeloos, E.; Marine, J.C.; Rambow, F. Epithelial-to-mesenchymal-like transition events in melanoma. FEBS J. 2022, 289, 1352–1368. [Google Scholar] [CrossRef]
- Li, J.; Yakushi, T.; Parlati, F.; Mackinnon, A.L.; Perez, C.; Ma, Y.; Carter, K.P.; Colayco, S.; Magnuson, G.; Brown, B.; et al. Capzimin is a potent and specific inhibitor of proteasome isopeptidase Rpn11. Nat. Chem. Biol. 2017, 13, 486–493. [Google Scholar] [CrossRef] [Green Version]
- Rabbie, R.; Ferguson, P.; Molina-Aguilar, C.; Adams, D.J.; Robles-Espinoza, C.D. Melanoma subtypes: Genomic profiles, prognostic molecular markers and therapeutic possibilities. J. Pathol. 2019, 247, 539–551. [Google Scholar] [CrossRef]
- Alkaraki, A.; McArthur, G.A.; Sheppard, K.E.; Smith, L.K. Metabolic Plasticity in Melanoma Progression and Response to Oncogene Targeted Therapies. Cancers 2021, 13, 5810. [Google Scholar] [CrossRef]
- Wajapeyee, N.; Gupta, R. Epigenetic Alterations and Mechanisms That Drive Resistance to Targeted Cancer Therapies. Cancer Res. 2021, 81, 5589–5595. [Google Scholar] [CrossRef]
- Turnbull, A.P.; Ioannidis, S.; Krajewski, W.W.; Pinto-Fernandez, A.; Heride, C.; Martin, A.C.L.; Tonkin, L.M.; Townsend, E.C.; Buker, S.M.; Lancia, D.R.; et al. Molecular basis of USP7 inhibition by selective small-molecule inhibitors. Nature 2017, 550, 481–486. [Google Scholar] [CrossRef]
- Mevissen, T.E.T.; Komander, D. Mechanisms of Deubiquitinase Specificity and Regulation. Annu. Rev. Biochem. 2017, 86, 159–192. [Google Scholar] [CrossRef] [Green Version]
- Doherty, L.M.; Mills, C.E.; Boswell, S.A.; Liu, X.; Hoyt, C.T.; Gyori, B.; Buhrlage, S.J.; Sorger, P.K. Integrating multi-omics data reveals function and therapeutic potential of deubiquitinating enzymes. eLife 2022, 11, e72879. [Google Scholar] [CrossRef] [PubMed]
- Krassikova, L.; Zhang, B.; Nagarajan, D.; Queiroz, A.L.; Kacal, M.; Samakidis, E.; Vakifahmetoglu-Norberg, H.; Norberg, E. The deubiquitinase JOSD2 is a positive regulator of glucose metabolism. Cell Death Differ. 2021, 28, 1091–1109. [Google Scholar] [CrossRef] [PubMed]
- Cockram, P.E.; Kist, M.; Prakash, S.; Chen, S.H.; Wertz, I.E.; Vucic, D. Ubiquitination in the regulation of inflammatory cell death and cancer. Cell Death Differ. 2021, 28, 591–605. [Google Scholar] [CrossRef] [PubMed]
- Iyengar, P.V. Regulation of Ubiquitin Enzymes in the TGF-beta Pathway. Int. J. Mol. Sci. 2017, 18, 877. [Google Scholar] [CrossRef] [Green Version]
- Gregoire-Mitha, S.; Gray, D.A. What deubiquitinating enzymes, oncogenes, and tumor suppressors actually do: Are current assumptions supported by patient outcomes? Bioessays 2021, 43, e2000269. [Google Scholar] [CrossRef]
- Datta, N.; Chakraborty, S.; Basu, M.; Ghosh, M.K. Tumor Suppressors Having Oncogenic Functions: The Double Agents. Cells 2020, 10, 46. [Google Scholar] [CrossRef]
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Ohanna, M.; Biber, P.; Deckert, M. Emerging Role of Deubiquitinating Enzymes (DUBs) in Melanoma Pathogenesis. Cancers 2022, 14, 3371. https://doi.org/10.3390/cancers14143371
Ohanna M, Biber P, Deckert M. Emerging Role of Deubiquitinating Enzymes (DUBs) in Melanoma Pathogenesis. Cancers. 2022; 14(14):3371. https://doi.org/10.3390/cancers14143371
Chicago/Turabian StyleOhanna, Mickael, Pierric Biber, and Marcel Deckert. 2022. "Emerging Role of Deubiquitinating Enzymes (DUBs) in Melanoma Pathogenesis" Cancers 14, no. 14: 3371. https://doi.org/10.3390/cancers14143371