OTUB1 promotes metastasis and serves as a marker of poor prognosis in colorectal cancer

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Zhou, Yi ^a   Wu, Jiangxue ^a   Fu, Xiang ^a   Du, Wuying ^a   Zhou, Ling ^a   Meng, Xiangqi ^a   Yu, Hongyan ^a   Lin, Jiaxin ^a   Ye, Wen ^a   Liu, Jiani ^a   Peng, Hui ^c   Liu, Ran yi ^a   Pan, Changchuan ^b   Huang, Wenlin ^a,d,e  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b SICHUAN CANCER HOSPITAL   (China)

^c THE SIXTH AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^d INSTITUTE OF MICROBIOLOGY   (China)

^e Science Park   (China)

Author keywords

Colorectal cancer; EMT; Metastasis; OTUB1; Prognostic factor

Indexed keywords

BETA CATENIN; DEUBIQUITINASE; PROTEIN OTUB1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CLASSIFICATION; CANCER LOCALIZATION; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CELL INVASION; CELL MIGRATION; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIVER METASTASIS; MAJOR CLINICAL STUDY; MALE; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION;

MUS;

EID: 84928267576     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-258     Document Type: Article

References (54)

1. Siegel R, Naishadham D, Jemal A: Cancer statistics, 2012. CA Cancer J Clin 1, 62:10-29. 10.3322/caac.20138
2. Spolverato G, Ejaz A, Azad N, Pawlik TM: Surgery for colorectal liver metastases: The evolution of determining prognosis. World J Gastrointest Oncol 2013, 5:207-221.
3. Andres A, Toso C, Adam R, Barroso E, Hubert C, Capussotti L, Gerstel E, Roth A, Majno PE, Mentha G: A survival analysis of the liver-first reversed management of advanced simultaneous colorectal liver metastases: a LiverMetSurvey-based study. Ann Surg 1, 256:772-779. 10.1097/SLA.0b013e3182734423
4. Mayo SC, Heckman JE, Shore AD, Nathan H, Parikh AA, Bridges JF, Anders RA, Anaya DA, Becker NS, Pawlik TM: Shifting trends in liver-directed management of patients with colorectal liver metastasis: a population-based analysis. Surgery 1, 150:204-216. 10.1016/j.surg.2011.06.013
5. Li X, Stevens PD, Yang H, Gulhati P, Wang W, Evers BM, Gao T: The deubiquitination enzyme USP46 functions as a tumor suppressor by controlling PHLPP-dependent attenuation of Akt signaling in colon cancer. Oncogene 1, 32:471-478. 10.1038/onc.2012.66
6. Liu YL, Yang YM, Xu H, Dong XS: Aberrant expression of USP22 is associated with liver metastasis and poor prognosis of colorectal cancer. J Surg Oncol 1, 103:283-289. 10.1002/jso.21802
7. Zhong J, Zhao M, Ma Y, Luo Q, Liu J, Wang J, Yuan X, Sang J, Huang C: UCHL1 acts as a colorectal cancer oncogene via activation of the beta-catenin/TCF pathway through its deubiquitinating activity. Int J Mol Med 2012, 30:430-436.
8. Harris DR, Mims A, Bunz F: Genetic disruption of USP9X sensitizes colorectal cancer cells to 5-fluorouracil. Cancer Biol Ther 1, 13:1319-1324. 10.4161/cbt.21792
9. Balakirev MY, Tcherniuk SO, Jaquinod M, Chroboczek J: Otubains: a new family of cysteine proteases in the ubiquitin pathway. EMBO Rep 1, 4:517-522. 10.1038/sj.embor.embor824
10. Wang T, Yin L, Cooper EM, Lai MY, Dickey S, Pickart CM, Fushman D, Wilkinson KD, Cohen RE, Wolberger C: Evidence for bidentate substrate binding as the basis for the K48 linkage specificity of otubain 1. J Mol Biol 1, 386:1011-1023. 10.1016/j.jmb.2008.12.085
11. Edelmann MJ, Iphofer A, Akutsu M, Altun M, di Gleria K, Kramer HB, Fiebiger E, Dhe-Paganon S, Kessler BM: Structural basis and specificity of human otubain 1-mediated deubiquitination. Biochem J 1, 418:379-390. 10.1042/BJ20081318
12. Juang YC, Landry MC, Sanches M, Vittal V, Leung CC, Ceccarelli DF, Mateo AR, Pruneda JN, Mao DY, Szilard RK, Orlicky S, Munro M, Brzovic PS, Klevit RE, Sicheri F, Durocher D: OTUB1 co-opts Lys48-linked ubiquitin recognition to suppress E2 enzyme function. Mol Cell 1, 45:384-397. 10.1016/j.molcel.2012.01.011
13. Blackford AN, Stewart GS: When cleavage is not attractive: non-catalytic inhibition of ubiquitin chains at DNA double-strand breaks by OTUB1. DNA Repair (Amst) 1, 10:245-249. 10.1016/j.dnarep.2010.11.004
14. Nakada S, Tai I, Panier S, Al-Hakim A, Iemura S, Juang YC, O'Donnell L, Kumakubo A, Munro M, Sicheri F, Gingras AC, Natsume T, Suda T, Durocher D: Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 1, 466:941-946. 10.1038/nature09297
15. Sato Y, Yamagata A, Goto-Ito S, Kubota K, Miyamoto R, Nakada S, Fukai S: Molecular basis of Lys-63-linked polyubiquitination inhibition by the interaction between human deubiquitinating enzyme OTUB1 and ubiquitin-conjugating enzyme UBC13. J Biol Chem 1, 287:25860-25868. 10.1074/jbc.M112.364752
16. Soares L, Seroogy C, Skrenta H, Anandasabapathy N, Lovelace P, Chung CD, Engleman E, Fathman CG: Two isoforms of otubain 1 regulate T cell anergy via GRAIL. Nat Immunol 2004, 5:45-54.
17. Herhaus L, Al-Salihi M, Macartney T, Weidlich S, Sapkota GP: OTUB1 enhances TGFbeta signalling by inhibiting the ubiquitylation and degradation of active SMAD2/3. Nat Commun 2013, 4:2519.
18. Goncharov T, Niessen K, de Almagro MC, Izrael-Tomasevic A, Fedorova AV, Varfolomeev E, Arnott D, Deshayes K, Kirkpatrick DS, Vucic D: OTUB1 modulates c-IAP1 stability to regulate signalling pathways. Embo J 1, 32:1103-1114. 10.1038/emboj.2013.62
19. Sun XX, Challagundla KB, Dai MS: Positive regulation of p53 stability and activity by the deubiquitinating enzyme Otubain 1. Embo J 1, 31:576-592. 10.1038/emboj.2011.434
20. Bolocan A, Ion D, Ciocan DN, Paduraru DN: Prognostic and predictive factors in colorectal cancer. Chirurgia (Bucur) 2012, 107:555-563.
21. Berg M, Agesen TH, Thiis-Evensen E, Merok MA, Teixeira MR, Vatn MH, Nesbakken A, Skotheim RI, Lothe RA: Distinct high resolution genome profiles of early onset and late onset colorectal cancer integrated with gene expression data identify candidate susceptibility loci. Mol Cancer 1, 9:100. 10.1186/1476-4598-9-100
22. Puvvada SD, Funkhouser WK, Greene K, Deal A, Chu H, Baldwin AS, Tepper JE, O'Neil BH: NF-kB and Bcl-3 activation are prognostic in metastatic colorectal cancer. Oncology 1, 78:181-188. 10.1159/000313697
23. Fakih MG, Padmanabhan A: CEA monitoring in colorectal cancer. What you should know. Oncology (Williston Park) 1, 20:579-587. discussion 588, 594, 596 passim
24. Yilmaz M, Christofori G, Lehembre F: Distinct mechanisms of tumor invasion and metastasis. Trends Mol Med 1, 13:535-541. 10.1016/j.molmed.2007.10.004
25. Reinacher-Schick A, Baldus SE, Romdhana B, Landsberg S, Zapatka M, Monig SP, Holscher AH, Dienes HP, Schmiegel W, Schwarte-Waldhoff I: Loss of Smad4 correlates with loss of the invasion suppressor E-cadherin in advanced colorectal carcinomas. J Pathol 1, 202:412-420. 10.1002/path.1516
26. Thiery JP, Sleeman JP: Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 1, 7:131-142. 10.1038/nrm1835
27. Berx G, Cleton-Jansen AM, Strumane K, de Leeuw WJ, Nollet F, van Roy F, Cornelisse C: E-cadherin is inactivated in a majority of invasive human lobular breast cancers by truncation mutations throughout its extracellular domain. Oncogene 1996, 13:1919-1925.
28. Baranwal S, Alahari SK: Molecular mechanisms controlling E-cadherin expression in breast cancer. Biochem Biophys Res Commun 1, 384:6-11. 10.1016/j.bbrc.2009.04.051
29. Carneiro P, Fernandes MS, Figueiredo J, Caldeira J, Carvalho J, Pinheiro H, Leite M, Melo S, Oliveira P, Simoes-Correia J, Oliveira MJ, Carneiro F, Figueiredo C, Paredes J, Oliveira C, Seruca R: E-cadherin dysfunction in gastric cancer-cellular consequences, clinical applications and open questions. FEBS Lett 1, 586:2981-2989. 10.1016/j.febslet.2012.07.045
30. Georgolios A, Eleftheriadou A, Batistatou A, Charalabopoulos K: Role of the recently identified dysadherin in E-cadherin adhesion molecule downregulation in head and neck cancer. Med Oncol 1, 29:1463-1467. 10.1007/s12032-011-0118-3
31. Salon C, Lantuejoul S, Eymin B, Gazzeri S, Brambilla C, Brambilla E: The E-cadherin-beta-catenin complex and its implication in lung cancer progression and prognosis. Future Oncol 1, 1:649-660. 10.2217/14796694.1.5.649
32. Wijnhoven BP, de Both NJ, van Dekken H, Tilanus HW, Dinjens WN: E-cadherin gene mutations are rare in adenocarcinomas of the oesophagus. Br J Cancer 1, 80:1652-1657. 10.1038/sj.bjc.6690577
33. Tsanou E, Peschos D, Batistatou A, Charalabopoulos A, Charalabopoulos K: The E-cadherin adhesion molecule and colorectal cancer. A global literature approach. Anticancer Res 2008, 28:3815-3826.
34. Buda A, Pignatelli M: E-cadherin and the cytoskeletal network in colorectal cancer development and metastasis. Cell Commun Adhes 1, 18:133-143. 10.3109/15419061.2011.636465
35. Schuhmacher C, Becker I, Oswald S, Atkinson MJ, Nekarda H, Becker KF, Mueller J, Siewert JR, Hofler H: Loss of immunohistochemical E-cadherin expression in colon cancer is not due to structural gene alterations. Virchows Arch 1, 434:489-495. 10.1007/s004280050373
36. Kwak JM, Min BW, Lee JH, Choi JS, Lee SI, Park SS, Kim J, Um JW, Kim SH, Moon HY: The prognostic significance of E-cadherin and liver intestine-cadherin expression in colorectal cancer. Dis Colon Rectum 1, 50:1873-1880. 10.1007/s10350-007-9034-1
37. Spaderna S, Schmalhofer O, Hlubek F, Berx G, Eger A, Merkel S, Jung A, Kirchner T, Brabletz T: A transient, EMT-linked loss of basement membranes indicates metastasis and poor survival in colorectal cancer. Gastroenterology 1, 131:830-840. 10.1053/j.gastro.2006.06.016
38. Eger A, Aigner K, Sonderegger S, Dampier B, Oehler S, Schreiber M, Berx G, Cano A, Beug H, Foisner R: DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 1, 24:2375-2385. 10.1038/sj.onc.1208429
39. Satelli A, Li S: Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell Mol Life Sci 1, 68:3033-3046. 10.1007/s00018-011-0735-1
40. Ngan CY, Yamamoto H, Seshimo I, Tsujino T, Man-i M, Ikeda JI, Konishi K, Takemasa I, Ikeda M, Sekimoto M, Matsuura N, Monden M: Quantitative evaluation of vimentin expression in tumour stroma of colorectal cancer. Br J Cancer 1, 96:986-992. 10.1038/sj.bjc.6603651
41. Shirahata A, Sakata M, Sakuraba K, Goto T, Mizukami H, Saito M, Ishibashi K, Kigawa G, Nemoto H, Sanada Y, Hibi K: Vimentin methylation as a marker for advanced colorectal carcinoma. Anticancer Res 2009, 29:279-281.
42. Yamasaki T, Seki N, Yamada Y, Yoshino H, Hidaka H, Chiyomaru T, Nohata N, Kinoshita T, Nakagawa M, Enokida H: Tumor suppressive microRNA138 contributes to cell migration and invasion through its targeting of vimentin in renal cell carcinoma. Int J Oncol 2012, 41:805-817.
43. Schmalhofer O, Brabletz S, Brabletz T: E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev 1, 28:151-166. 10.1007/s10555-008-9179-y
44. Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW, Vogelstein B, Clevers H: Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 1, 275:1784-1787. 10.1126/science.275.5307.1784
45. Brabletz T, Herrmann K, Jung A, Faller G, Kirchner T: Expression of nuclear beta-catenin and c-myc is correlated with tumor size but not with proliferative activity of colorectal adenomas. Am J Pathol 1, 156:865-870. 10.1016/S0002-9440(10)64955-3
46. Wong SC, Lo ES, Lee KC, Chan JK, Hsiao WL: Prognostic and diagnostic significance of beta-catenin nuclear immunostaining in colorectal cancer. Clin Cancer Res 1, 10:1401-1408. 10.1158/1078-0432.CCR-0157-03
47. Doble BW, Woodgett JR: GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 1, 116:1175-1186. 10.1242/jcs.00384
48. Munemitsu S, Albert I, Souza B, Rubinfeld B, Polakis P: Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci U S A 1, 92:3046-3050. 10.1073/pnas.92.7.3046
49. Simcha I, Shtutman M, Salomon D, Zhurinsky J, Sadot E, Geiger B, Ben-Ze'ev A: Differential nuclear translocation and transactivation potential of beta-catenin and plakoglobin. J Cell Biol 1, 141:1433-1448. 10.1083/jcb.141.6.1433
50. Abubaker J, Bavi P, Al-Haqawi W, Jehan Z, Munkarah A, Uddin S, Al-Kuraya KS: PIK3CA alterations in Middle Eastern ovarian cancers. Mol Cancer 1, 8:51. 10.1186/1476-4598-8-51
51. Cai MY, Luo RZ, Chen JW, Pei XQ, Lu JB, Hou JH, Yun JP: Overexpression of ZEB2 in peritumoral liver tissue correlates with favorable survival after curative resection of hepatocellular carcinoma. PLoS One 1, 7:e32838. 10.1371/journal.pone.0032838
52. Wang H, Wu J, Meng X, Ying X, Zuo Y, Liu R, Pan Z, Kang T, Huang W: MicroRNA-342 inhibits colorectal cancer cell proliferation and invasion by directly targeting DNA methyltransferase 1. Carcinogenesis 1, 32:1033-1042. 10.1093/carcin/bgr081
53. Meng X, Wu J, Pan C, Wang H, Ying X, Zhou Y, Yu H, Zuo Y, Pan Z, Liu RY, Huang W: Genetic and epigenetic down-regulation of microRNA-212 promotes colorectal tumor metastasis via dysregulation of MnSOD. Gastroenterology 1, 145:426-436. e421-426 10.1053/j.gastro.2013.04.004
54. Huang S, Jean D, Luca M, Tainsky MA, Bar-Eli M: Loss of AP-2 results in downregulation of c-KIT and enhancement of melanoma tumorigenicity and metastasis. Embo J 1, 17:4358-4369. 10.1093/emboj/17.15.4358