USP22 promotes NSCLC tumorigenesis via MDMX up-regulation and subsequent p53 inhibition

International Journal of Molecular Sciences

Volumn 16, Issue 1, 2015, Pages 307-320

  Ding, Fangbao ^a   Bao, Chunrong ^a   Tian, Yue ^b   Xiao, Haibo ^a   Wang, Mingsong ^a   Xie, Xiao ^a   Hu, Fengqing ^a   Mei, Ju ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

MDMX; NSCLC; P53; USP22

Indexed keywords

DEUBIQUITINASE; MESSENGER RNA; PROTEIN MDMX; PROTEIN P53; UBIQUITIN SPECIFIC PROTEASE 22; UNCLASSIFIED DRUG; MDM4 PROTEIN, HUMAN; NUCLEAR PROTEIN; ONCOPROTEIN; PROTEIN BINDING; THIOL ESTER HYDROLASE; USP22 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL CYCLE ARREST; CELL CYCLE ASSAY; CELL CYCLE G0 PHASE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; MALE; MOUSE; MTT ASSAY; NON SMALL CELL LUNG CANCER; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR GROWTH; UPREGULATION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; GENETICS; LUNG TUMOR; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CARCINOGENESIS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; NUCLEAR PROTEINS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; THIOLESTER HYDROLASES; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84919783983     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16010307     Document Type: Article

References (37)

1. Ferlay, J.; Shin, H. R.; Bray, F.; Forman, D.; Mathers, C.; Parkin, D. M. Estimates of worldwide burden of cancer in 2008: Globocan 2008. Int. J. Cancer 2010, 127, 2893-2917.
2. Siegel, R.; DeSantis, C.; Virgo, K.; Stein, K.; Mariotto, A.; Smith, T.; Cooper, D.; Gansler, T.; Lerro, C.; Fedewa, S.; et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J. Clin. 2012, 62, 220-241.
3. Herbst, R. S.; Heymach, J. V.; Lippman, S. M. Lung cancer. N. Engl. J. Med. 2008, 359, 1367-1380.
4. Mascaux, C.; Shepherd, F. A. Adjuvant chemotherapy after pulmonary resection for lung cancer. Thoracic Surg. Clin. 2013, 23, 401-410.
5. Binder, D.; Hegenbarth, K. Emerging options for the management of non-small cell lung cancer. Clin. Med. Insights Oncol. 2013, 7, 221-234.
6. Zarogoulidis, K.; Zarogoulidis, P.; Darwiche, K.; Boutsikou, E.; Machairiotis, N.; Tsakiridis, K.; Katsikogiannis, N.; Kougioumtzi, I.; Karapantzos, I.; Huang, H.; et al. Treatment of non-small cell lung cancer (nsclc). J. Thoracic Dis. 2013, 5, S389-S396.
7. Bonnet, J.; Romier, C.; Tora, L.; Devys, D. Zinc-finger ubps: Regulators of deubiquitylation. Trends Biochem. Sci. 2008, 33, 369-375.
8. Glinsky, G. V.; Berezovska, O.; Glinskii, A. B. Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. J. Clin. Investig. 2005, 115, 1503-1521.
9. Zhang, X. Y.; Varthi, M.; Sykes, S. M.; Phillips, C.; Warzecha, C.; Zhu, W.; Wyce, A.; Thorne, A. W.; Berger, S. L.; McMahon, S. B. The putative cancer stem cell marker usp22 is a subunit of the human saga complex required for activated transcription and cell-cycle progression. Mol. Cell 2008, 29, 102-111.
10. Zhang, X. Y.; Pfeiffer, H. K.; Thorne, A. W.; McMahon, S. B. Usp22, an hsaga subunit and potential cancer stem cell marker, reverses the polycomb-catalyzed ubiquitylation of histone h2a. Cell Cycle 2008, 7, 1522-1524.
11. Liu, Y. L.; Jiang, S. X.; Yang, Y. M.; Xu, H.; Liu, J. L.; Wang, X. S. Usp22 acts as an oncogene by the activation of bmi-1-mediated ink4a/arf pathway and akt pathway. Cell Biochem. Biophys. 2012, 62, 229-235.
12. Lin, Z.; Yang, H.; Kong, Q.; Li, J.; Lee, S. M.; Gao, B.; Dong, H.; Wei, J.; Song, J.; Zhang, D. D.; et al. Usp22 antagonizes p53 transcriptional activation by deubiquitinating sirt1 to suppress cell apoptosis and is required for mouse embryonic development. Mol. Cell 2012, 46, 484-494.
13. Lv, L.; Xiao, X. Y.; Gu, Z. H.; Zeng, F. Q.; Huang, L. Q.; Jiang, G. S. Silencing usp22 by asymmetric structure of interfering rna inhibits proliferation and induces cell cycle arrest in bladder cancer cells. Mol. Cell. Biochem. 2011, 346, 11-21.
14. Liu, Y. L.; Yang, Y. M.; Xu, H.; Dong, X. S. Increased expression of ubiquitin-specific protease 22 can promote cancer progression and predict therapy failure in human colorectal cancer. J. Gastroenterol. Hepatol. 2010, 25, 1800-1805.
15. Hu, J.; Liu, Y. L.; Piao, S. L.; Yang, D. D.; Yang, Y. M.; Cai, L. Expression patterns of usp22 and potential targets bmi-1, pten, p-akt in non-small-cell lung cancer. Lung Cancer 2012, 77, 593-599.
16. Yang, D. D.; Cui, B. B.; Sun, L. Y.; Zheng, H. Q.; Huang, Q.; Tong, J. X.; Zhang, Q. F. The co-expression of usp22 and bmi-1 may promote cancer progression and predict therapy failure in gastric carcinoma. Cell Biochem. Biophys. 2011, 61, 703-710.
17. Ning, J.; Zhang, J.; Liu, W.; Lang, Y.; Xue, Y.; Xu, S. Overexpression of ubiquitin-specific protease 22 predicts poor survival in patients with early-stage non-small cell lung cancer. Eur. J. Histochem. 2012, 56, e46.
18. Wang, H.; Li, Y. P.; Chen, J. H.; Yuan, S. F.; Wang, L.; Zhang, J. L.; Yao, Q.; Li, N. L.; Bian, J. F.; Fan, J.; et al. Prognostic significance of usp22 as an oncogene in papillary thyroid carcinoma. Tumour Biol. J. Int. Soc. Oncodev. Biol. Med. 2013, 34, 1635-1639.
19. Piao, S.; Liu, Y.; Hu, J.; Guo, F.; Ma, J.; Sun, Y.; Zhang, B. Usp22 is useful as a novel molecular marker for predicting disease progression and patient prognosis of oral squamous cell carcinoma. PLoS One 2012, 7, e42540.
20. Yang, M.; Liu, Y. D.; Wang, Y. Y.; Liu, T. B.; Ge, T. T.; Lou, G. Ubiquitin-specific protease 22: A novel molecular biomarker in cervical cancer prognosis and therapeutics. Tumour Biol. J. Int. Soc. Oncodev. Biol. Med. 2014, 35, 929-934.
21. Van Zandwijk, N.; Mooi, W. J.; Rodenhuis, S. Prognostic factors in nsclc. Recent experiences. Lung Cancer 1995, 12, S27-S33.
22. Stegh, A. H. Targeting the p53 signaling pathway in cancer therapy-The promises, challenges and perils. Exp. Opin. Ther. Targets 2012, 16, 67-83.
23. Wang, X. P53 regulation: Teamwork between ring domains of mdm2 and mdmx. Cell Cycle 2011, 10, 4225-4229.
24. Wade, M.; Li, Y. C.; Wahl, G. M. Mdm2, mdmx and p53 in oncogenesis and cancer therapy. Nat. Rev. Cancer 2013, 13, 83-96.
25. Brown, C. J.; Lain, S.; Verma, C. S.; Fersht, A. R.; Lane, D. P. Awakening guardian angels: Drugging the p53 pathway. Nat. Rev. Cancer 2009, 9, 862-873.
26. Ray-Coquard, I.; Blay, J. Y.; Italiano, A.; le Cesne, A.; Penel, N.; Zhi, J.; Heil, F.; Rueger, R.; Graves, B.; Ding, M.; et al. Effect of the mdm2 antagonist rg7112 on the p53 pathway in patients with mdm2-amplified, well-differentiated or dedifferentiated liposarcoma: An exploratory proof-of-mechanism study. Lancet Oncol. 2012, 13, 1133-1140.
27. Yang, Y.; Ludwig, R. L.; Jensen, J. P.; Pierre, S. A.; Medaglia, M. V.; Davydov, I. V.; Safiran, Y. J.; Oberoi, P.; Kenten, J. H.; Phillips, A. C.; et al. Small molecule inhibitors of hdm2 ubiquitin ligase activity stabilize and activate p53 in cells. Cancer Cell 2005, 7, 547-559.
28. Roxburgh, P.; Hock, A. K.; Dickens, M. P.; Mezna, M.; Fischer, P. M.; Vousden, K. H. Small molecules that bind the mdm2 ring stabilize and activate p53. Carcinogenesis 2012, 33, 791-798.
29. Herman, A. G.; Hayano, M.; Poyurovsky, M. V.; Shimada, K.; Skouta, R.; Prives, C.; Stockwell, B. R. Discovery of mdm2-mdmx e3 ligase inhibitors using a cell-based ubiquitination assay. Cancer Discov. 2011, 1, 312-325.
30. Wang, H.; Ma, X.; Ren, S.; Buolamwini, J. K.; Yan, C. A small-molecule inhibitor of mdmx activates p53 and induces apoptosis. Mol. Cancer Ther. 2011, 10, 69-79.
31. Vaseva, A. V.; Yallowitz, A. R.; Marchenko, N. D.; Xu, S.; Moll, U. M. Blockade of hsp90 by 17aag antagonizes mdmx and synergizes with nutlin to induce p53-mediated apoptosis in solid tumors. Cell Death Dis. 2011, 2, e156.
32. Li, M.; Brooks, C. L.; Kon, N.; Gu, W. A dynamic role of hausp in the p53-mdm2 pathway. Mol. Cell 2004, 13, 879-886.
33. Colland, F.; Formstecher, E.; Jacq, X.; Reverdy, C.; Planquette, C.; Conrath, S.; Trouplin, V.; Bianchi, J.; Aushev, V. N.; Camonis, J.; et al. Small-molecule inhibitor of usp7/hausp ubiquitin protease stabilizes and activates p53 in cells. Mol. Cancer Ther. 2009, 8, 2286-2295.
34. Kim, J.; Keay, S. K.; You, S.; Loda, M.; Freeman, M. R. A synthetic form of frizzled 8-associated antiproliferative factor enhances p53 stability through usp2a and mdm2. PLoS One 2012, 7, e50392.
35. Hoeller, D.; Dikic, I. Targeting the ubiquitin system in cancer therapy. Nature 2009, 458, 438-444.
36. Sacco, J. J.; Coulson, J. M.; Clague, M. J.; Urbe, S. Emerging roles of deubiquitinases in cancer-associated pathways. IUBMB Life 2010, 62, 140-157.
37. Schrecengost, R. S.; Dean, J. L.; Goodwin, J. F.; Schiewer, M. J.; Urban, M. W.; Stanek, T. J.; Sussman, R. T.; Hicks, J. L.; Birbe, R. C.; Draganova-Tacheva, R. A.; et al. Usp22 regulates oncogenic signaling pathways to drive lethal cancer progression. Cancer Res. 2014, 74, 272-286.