The ISG15-specific protease USP18 regulates stability of PTEN

Oncotarget

Volumn 8, Issue 1, 2017, Pages 3-14

  Mustachio, Lisa Maria ^a   Kawakami, Masanori ^b   Lu, Yun ^a   Rodriguez Canales, Jaime ^b   Mino, Barbara ^b   Behrens, Carmen ^b   Wistuba, Ignacio ^b   Bota Rabassedas, Neus ^b   Yu, Jun ^b   Jack Lee, J ^b   Roszik, Jason ^b   Zheng, Lin ^b   Liu, Xi ^b   Freemantle, Sarah J ^a   Dmitrovsky, Ethan ^a,b  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

And lung cancer; ISG15; Protein stability; PTEN; USP18

Indexed keywords

CYTOKINE; ISG15 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEINASE; UBIQUITIN; UBIQUITIN THIOLESTERASE; USP18 PROTEIN, HUMAN;

ANIMAL; GENE KNOCKOUT; GENETICS; HUMAN; LUNG TUMOR; METABOLISM; MOUSE; PROTEIN PROCESSING; PROTEIN STABILITY; TUMOR CELL LINE; UBIQUITINATION;

ANIMALS; CELL LINE, TUMOR; CYTOKINES; ENDOPEPTIDASES; GENE KNOCKOUT TECHNIQUES; HUMANS; LUNG NEOPLASMS; MICE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PTEN PHOSPHOHYDROLASE; UBIQUITIN THIOLESTERASE; UBIQUITINATION; UBIQUITINS;

EID: 85009476576     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.13914     Document Type: Article

References (45)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016; 66: 7-30.
2. Romanidou O, Landi L, Cappuzzo F, Califano R. Overcoming resistance to first/second generation epidermal growth factor receptor tyrosine kinase inhibitors and ALK inhibitors in oncogene-addicted advanced non-small cell lung cancer. Ther Adv Med Oncol. 2016; 8: 176-87.
3. Burger AM, Seth AK. The ubiquitin-mediated protein degradation pathway in cancer: therapeutic implications. Eur J Cancer. 2004; 40: 2217-29.
4. Herrmann J, Lerman LO, Lerman A. Ubiquitin and ubiquitin-like proteins in protein regulation. Circ Res. 2007; 100: 1276-91.
5. Leslie NR, Downes CP. PTEN function: how normal cells control it and tumour cells lose it. Biochem J. 2004; 382: 1-11.
6. Jin G, Kim MJ, Jeon HS, Choi JE, Kim DS, Lee EB, Cha SI, Yoon GS, Kim CH, Jung TH, Park JY. PTEN mutations and relationship to EGFR, ERBB2, KRAS, and TP53 mutations in non-small cell lung cancers. Lung Cancer. 2010; 69: 279-83.
7. Hollander MC, Blumenthal GM, Dennis PA. PTEN loss in the continuum of common cancers, rare syndromes and mouse models. Nat Rev Cancer. 2011; 11: 289-301.
8. Shi Y, Paluch BE, Wang X, Jiang X. PTEN at a glance. J Cell Sci. 2012; 125: 4687-92.
9. Song MS, Salmena L, Carracedo A, Egia A, Lo-Coco F, Teruya-Feldstein J, PandolfiPP. The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network. Nature. 2008; 455: 813-7.
10. Zhang J, Zhang P, Wei Y, Piao HL, Wang W, Maddika S, Wang M, Chen D, Sun Y, Hung MC, Chen J, Ma L. Deubiquitylation and stabilization of PTEN by USP13. Nat Cell Biol. 2013; 15: 1486-94.
11. Dao CT, Zhang DE. ISG15: a ubiquitin-like enigma. Front Biosci. 2005; 10: 2701-22.
12. Yuan WM, Krug RM. Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 2011; 20: 362-71.
13. Zhao C, Beaudenon SL, Kelley ML, Waddell MB, Yuan W, Schulman BA, Huibregtse JM, Krug RM. The UbcH8 ubiquitin E2 enzyme is also the E2 enzyme for ISG15, an IFN-alpha/beta-induced ubiquitin-like protein. Proc Natl Acad Sci U S A. 2004; 101: 7578-82.
14. Wong JJ, Pung YF, Sze NS, Chin KC. HERC5 is an IFNinduced HECT-type E3 protein ligase that mediates type I IFN-induced ISGylation of protein targets. Proc Natl Acad Sci (USA). 2006; 103: 10735-40.
15. Malakhov MP, Malakhova OA, Kim KI, Ritchie KJ, Zhang DE. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J Biol Chem. 2002; 277: 9976-81.
16. Feng Q, Sekula D, Guo Y, Liu X, Black CC, Galimberti F, Shah SJ, Sempere LF, Memoli V, Andersen JB, Hassel BA, Dragnev K, Dmitrovsky E. UBE1L causes lung cancer growth suppression by targeting cyclin D1. Mol Cancer Ther. 2008; 7: 3780-88.
17. Shah SJ, Blumen S, Pitha-Rowe I, Kitareewan S, Freemantle SJ, Feng Q, Dmitrovsky E. UBE1L represses PML/RARa by targeting the PML domain for ISG15ylation. Mol Cancer Ther. 2008; 7: 905-14.
18. Knobeloch KP. In vivo functions of ISGylation. In: Groettrup M, editor. Conjugation and deconjugation of ubiquitin family modifiers. Austin, Texas, USA: Landes Bioscience; 2010. P. 215-27.
19. Guo Y, Chinyengetere F, Dolinko AV, Lopez-Aguiar A, Lu Y, Galimberti F, Ma T, Feng Q, Sekula D, Freemantle SJ, Andrew AS, Memoli V, Dmitrovsky E. Evidence for the ubiquitin protease UBP43 as an antineoplastic target. Mol Cancer Ther. 2012; 11: 1968-77.
20. Guo Y, Dolinko AV, Chinyengetere F, Stanton B, Bomberger JM, Demidenko E, Zhou DC, Gallagher R, Ma T, Galimberti F, Liu X, Sekula D, Freemantle S, et al. Blockade of the ubiquitin protease UBP43 destabilizes the transcription factor PML/RARa and inhibits growth of acute promyelocytic leukemia. Cancer Res. 2010; 70: 9875-85.
21. Chinyengetere F, Sekula DJ, Lu Y, Giustini AJ, Sanglikar A, Kawakami M, Burkett SS, Eisenberg BL, Wells WA, Hoopes PJ, Demicco EG, Lazar AJ, Torres KE, et al. Mice null for the deubiquitinase USP18 spontaneously develop leiomyosarcomas. BMC Cancer. 2015; 15: 886-98.
22. Durfee LA, Huibregtse JM. Identification and validation of ISG15 target proteins. Subcell Biochem. 2010; 54: 228-37.
23. Wu RC, Wang TL, Shih leM. The emerging roles of ARID1A in tumor suppression. Cancer Biol Ther. 2014; 15: 655-64.
24. Wu JN, Roberts CWM. ARID1A mutations in cancer: another epigenetic tumor suppressor? Cancer Discov. 2013; 3: 35-43.
25. Wang DD, Chen YB, Pan K, Wang W, Chen SP, Chen JG, Zhao JJ, Lv L, Pan QZ, Li YQ, Wang QJ, Huang LX, Ke ML, et al. Decreased expression of the ARID1A gene is associated with poor prognosis in primary gastric cancer. PLoS One. 2012; 7: e40364.
26. He F, Li J, Xu J, Zhang S, Xu Y, Zhao W, Yin Z, Wang X. Decreased expression of ARID1A associates with poor prognosis and promotes metastases of hepatocellular carcinoma. J Exp Clin Cancer Res. 2015; 34: 47.
27. Chen Y, Zheng J, Yang X, Sun L, Xin Y. Effects of mutation and expression of PTEN gene mRNA on tumorigenesis and progression of epithelial ovarian cancer. Chin Med Sci J. 2004; 19: 25-30.
28. Malakhova OA, Yan M, Malakhov MP, Yuan Y, Ritchie KJ, Kim KI, Peterson LF, Shuai K, Zhang DE. Protein ISGylation modulates the JAK-STAT signaling pathway. Genes Dev. 2003; 17: 455-60.
29. Kim MJ, Yoo JY. Inhibition of hepatitis C virus replication by IFN-mediated ISGylation of HCV-NS5A. J Immunol. 2010; 85: 4311-8.
30. Burkart C, Fan JB, Zhang DE. Two independent mechanisms promote expression of an N-terminal truncated USP18 isoform with higher deISGylation activity in the nucleus. J Biol Chem. 2012; 287: 4883-93.
31. Trotman LC, Wang X, Alimonti A, Chen Z, Teruya-Feldstein J, Yang H, Pavletich NP, Carver BS, Cordon-Cardo C, Erdjument-Bromage H, Tempst P, Chi SG, Kim HJ, et al. Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell. 2007; 128: 141-56.
32. Nakashima H, Nguyen T, Goins WF, Chiocca EA. Interferon-stimulated gene 15 (ISG15) and ISG15-linked proteins can associate with members of the selective autophagic process, histone deacetylase 6 (HDAC6) and SQSTM1/p62. J Biol Chem. 2015; 290: 1485-95.
33. Huang YF, Wee S, Gunaratne J, Lane DP, Bulavin DV. Isg15 controls p53 stability and functions. Cell Cycle. 2014; 13: 2200-10.
34. Krueger KE, Srivastava S. Posttranslational protein modifications: current implications for cancer detection, prevention, and therapeutics. Mol Cell Proteomics. 2006; 5: 1799-810.
35. Zhao C, Hsiang TY, Kuo RL, Krug RM. ISG15 conjugation system targets the viral NS1 protein in influenza A virusinfected cells. Proc Natl Acad Sci (USA). 2010; 107: 2253-58.
36. Desai SD. ISG15: A double edged sword in cancer. Oncoimmunology. 2015; 4: e1052935.
37. Planchon SM, Waite KA, Eng C. The nuclear affairs of PTEN. J Cell Sci. 2008; 121: 249-53.
38. Sacco JJ, Coulson JM, Clague MJ, Urbé S. Emerging roles of deubiquitinases in cancer-associated pathways. IUBMB Life. 2010; 62: 140-57.
39. Sheng Y, Saridakis V, Sarkari F, Duan S, Wu T, Arrowsmith CH, Frappier L. Molecular recognition of p53 and MDM2 by USP7/HAUSP. Nat Struct Mol Biol. 2006; 13: 285-91.
40. Zhang D, Zhang D. Interferon-stimulated gene 15 and the protein ISGylation system. J Interferon Cytokine Res. 2011; 31: 119-30.
41. Guijarro MV, Dahiya S, Danielson LS, Segura MF, Vales-Lara FM, Menendez S, Popiolek D, Mittal K, Wei JJ, Zavadil J, Cordon-Cardo C, PandolfiPP, Hernando E. Dual Pten/Tp53 suppression promotes sarcoma progression by activating Notch signaling. Am J Pathol. 2013; 182: 2015-27.
42. Liu X, Sempere LF, Ouyang H, Memoli VA, Andrew AS, Luo Y, Demidenko E, Korc M, Shi W, Preis M, Dragnev KH, Li H, Direnzo J, et al. MicroRNA-31 functions as an oncogenic microRNA in mouse and human lung cancer cells by repressing specific tumor suppressors. J Clin Invest. 2010; 120: 1298-309.
43. Wislez M, Fujimoto N, Izzo JG, Hanna AE, Cody DD, Langley RR, Tang H, Burdick MD, Sato M, Minna JD, Mao L, Wistuba I, Strieter RM, et al. High expression of ligands for chemokine receptor CXCR2 in alveolar epithelial neoplasia induced by oncogenic kras. Cancer Res. 2006; 66: 4198-207.
44. Tibes R, Qiu Y, Lu Y, Hennessy B, AndreeffM, Mills GB, Kornblau SM. Reverse phase protein array: validation of a novel proteomic technology and utility for analysis of primary leukemia specimens and hematopoietic stem cells. Mol Cancer Ther. 2006; 5: 2512-21.
45. Wagner GP, Kin K, Lynch VJ. Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci. 2012; 131: 281-85.