Ubiquitin-conjugating enzyme UBE2C: Molecular biology, role in tumorigenesis, and potential as a biomarker

Tumor Biology

Volumn 33, Issue 3, 2012, Pages 723-730

  Hao, Zhonglin ^a   Zhang, Hui ^a   Cowell, John ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Cancer; Checkpoint; Genomic instability; Prognosis; UBE2C

Indexed keywords

CYCLIN B; LYSINE; MYC PROTEIN; TUMOR MARKER; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN CONJUGATING ENZYME 2C; UNCLASSIFIED DRUG;

CANCER SURVIVAL; CARCINOGENESIS; CELL CYCLE; CELL CYCLE CHECKPOINT; CHROMOSOME; DISEASE MARKER; ENZYME REGULATION; GENOMIC INSTABILITY; GLIOMA; HEMATOLOGIC MALIGNANCY; HUMAN; MALIGNANT TRANSFORMATION; MITOSIS; MITOSIS SPINDLE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RELAPSE; REVIEW; SOLID TUMOR; THYROID CANCER; UBIQUITINATION; UPREGULATION; ANIMAL; CELL TRANSFORMATION; GENETICS; METABOLISM; NEOPLASM;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; NEOPLASMS; TUMOR MARKERS, BIOLOGICAL; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84863602520     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-011-0291-1     Document Type: Review

References (68)

1. Jesenberger V, Jentsch S. Deadly encounter: ubiquitin meets apoptosis. Nat Rev Mol Cell Biol. 2002;3(2):112-21.
2. Williamson A, Wickliffe KE, Mellone BG, Song L, Karpen GH, Rape M. Identification of a physiological E2 module for the human anaphase-promoting complex. Proc Natl Acad Sci USA. 2009;106(43):18213-8.
3. Kerscher O, Felberbaum R, Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol. 2006;22:159-80.
4. Liu YC. Ubiquitin ligases and the immune response. Annu Rev Immunol. 2004;22:81-127.
5. Kimura Y, Tanaka K. Regulatory mechanisms involved in the control of ubiquitin homeostasis. J Biochem. 2010;147(6):793-8.
6. Hicke L, Schubert HL, Hill CP. Ubiquitin-binding domains. Nat Rev Mol Cell Biol. 2005;6(8):610-21.
7. Stegmeier F, Rape M, Draviam VM, Nalepa G, Sowa ME, Ang XL, et al. Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature. 2007;446(7138):876-81.
8. Reddy SK, Rape M, Margansky WA, Kirschner MW. Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature. 2007;446(7138):921-5.
9. van Ree JH, Jeganathan KB, Malureanu L, van Deursen JM. Overexpression of the E2 ubiquitin-conjugating enzyme UbcH10 causes chromosome missegregation and tumor formation. J Cell Biol. 2010;188(1):83-100.
10. Townsley FM, Aristarkhov A, Beck S, Hershko A, Ruderman JV. Dominant-negative cyclin-selective ubiquitin carrier protein E2-C/UbcH10 blocks cells in metaphase. Proc Natl Acad Sci USA. 1997;94(6):2362-7.
11. Kim S, Yu H. Mutual regulation between the spindle checkpoint and APC/C. Semin Cell Dev Biol. 2011;22(6):551-8.
12. Nath S, Banerjee T, Sen D, Das T, Roychoudhury S. Spindle assembly checkpoint protein Cdc20 transcriptionally activates expression of ubiquitin carrier protein UbcH10. J Biol Chem. 2011;286(18):15666-77.
13. Gauci S, Helbig AO, Slijper M, Krijgsveld J, Heck AJ, Mohammed S. Lys-N and trypsin cover complementary parts of the phosphoproteome in a refined SCX-based approach. Anal Chem. 2009;81(11):4493-501.
14. Rape M, Kirschner MW. Autonomous regulation of the anaphasepromoting complex couples mitosis to S-phase entry. Nature. 2004;432(7017):588-95.
15. Jin L, Williamson A, Banerjee S, Philipp I, Rape M. Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell. 2008;133(4):653-65.
16. David Y, Ziv T, Admon A, Navon A. The E2 ubiquitin-conjugating enzymes direct polyubiquitination to preferred lysines. J Biol Chem. 2010;285(12):8595-604.
17. Nasmyth K. How do so few control so many? Cell. 2005;120(6):739-46.
18. Yanagida M. Basic mechanism of eukaryotic chromosome segregation. Philos Trans R Soc Lond B Biol Sci. 2005;360(1455):609-21.
19. Fang G. Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex. Mol Biol Cell. 2002;13(3):755-66.
20. Wickliffe KE, Lorenz S, Wemmer DE, Kuriyan J, Rape M. The mechanism of linkage-specific ubiquitin chain elongation by a single-subunit E2. Cell. 2011;144(5):769-81.
21. Murray AW. Recycling the cell cycle: cyclins revisited. Cell. 2004;116(2):221-34.
22. Jackson PK, Eldridge AG, Freed E, Furstenthal L, Hsu JY, Kaiser BK, et al. The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol. 2000;10(10):429-39.
23. Jiang F, Basavappa R. Crystal structure of the cyclin-specific ubiquitin-conjugating enzyme from clam, E2-C, at 2.0 A resolution. Biochemistry. 1999;38(20):6471-8.
24. Lin Y, Hwang WC, Basavappa R. Structural and functional analysis of the human mitotic-specific ubiquitin-conjugating enzyme, UbcH10. J Biol Chem. 2002;277(24):21913-21.
25. Summers MK, Pan B, Mukhyala K, Jackson PK. The unique N terminus of the UbcH10 E2 enzyme controls the threshold for APC activation and enhances checkpoint regulation of the APC. Mol Cell. 2008;31(4):544-56.
26. Okamoto Y, Ozaki T, Miyazaki K, Aoyama M, Miyazaki M, Nakagawara A. UbcH10 is the cancer-related E2 ubiquitinconjugating enzyme. Cancer Res. 2003;63(14):4167-73.
27. May WA, Arvand A, Thompson AD, Braun BS, Wright M, Denny CT. EWS/FLI1-induced manic fringe renders NIH 3T3 cells tumorigenic. Nat Genet. 1997;17(4):495-7.
28. Sudbo J, Lippman SM, Lee JJ, Mao L, Kildal W, Sudbo A, et al. The influence of resection and aneuploidy on mortality in oral leukoplakia. N Engl J Med. 2004;350(14):1405-13.
29. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-74.
30. Kadara H, Behrens C, Yuan P, Solis L, Liu D, Gu X, et al. A five-gene and corresponding protein signature for stage-I lung adenocarcinoma prognosis. Clin Cancer Res. 2011;17(6):1490-501.
31. Hunter KD, Thurlow JK, Fleming J, Drake PJ, Vass JK, Kalna G, et al. Divergent routes to oral cancer. Cancer Res. 2006;66(15):7405-13.
32. Patel D, Mc Cance DJ. Compromised spindle assembly checkpoint due to altered expression of Ubch10 and Cdc20 in human papillomavirus type 16 E6-and E7-expressing keratinocytes. J Virol. 2010;84(21):10956-64.
33. Wagner KW, Sapinoso LM, El-Rifai W, Frierson HF, Butz N, Mestan J, et al. Overexpression, genomic amplification and therapeutic potential of inhibiting the UbcH10 ubiquitin conjugase in human carcinomas of diverse anatomic origin. Oncogene. 2004;23(39):6621-9.
34. Berlingieri MT, Pallante P, Sboner A, Barbareschi M, Bianco M, Ferraro A, et al. UbcH10 is overexpressed in malignant breast carcinomas. Eur J Cancer. 2007;43(18):2729-35.
35. Loussouarn D, Campion L, Leclair F, Campone M, Charbonnel C, Ricolleau G, et al. Validation of UBE2C protein as a prognostic marker in node-positive breast cancer. Br J Cancer. 2009;101(1):166-73.
36. Berlingieri MT, Pallante P, Guida M, Nappi C, Masciullo V, Scambia G, et al. UbcH10 expression may be a useful tool in the prognosis of ovarian carcinomas. Oncogene. 2007;26(14):2136-40.
37. Chen S, Chen Y, Hu C, Jing H, Cao Y, Liu X. Association of clinicopathological features with UbcH10 expression in colorectal cancer. J Cancer Res Clin Oncol. 2010;136(3):419-26.
38. Ieta K, Ojima E, Tanaka F, Nakamura Y, Haraguchi N, Mimori K, et al. Identification of overexpressed genes in hepatocellular carcinoma, with special reference to ubiquitin-conjugating enzyme E2C gene expression. Int J Cancer. 2007;121(1):33-8.
39. Pallante P, Berlingieri MT, Troncone G, Kruhoffer M, Orntoft TF, Viglietto G, et al. UbcH10 overexpression may represent a marker of anaplastic thyroid carcinomas. Br J Cancer. 2005;93(4):464-71.
40. Jiang L, Huang CG, Lu YC, Luo C, Hu GH, Liu HM, et al. Expression of ubiquitin-conjugating enzyme E2C/UbcH10 in astrocytic tumors. Brain Res. 2008;1201:161-6.
41. Wang Q, Li W, Zhang Y, Yuan X, Xu K, Yu J, et al. Androgen receptor regulates a distinct transcription program in androgenindependent prostate cancer. Cell. 2009;138(2):245-56.
42. Chen Z, Zhang C, Wu D, Chen H, Rorick A, Zhang X, et al. Phospho-MED1-enhanced UBE2C locus looping drives castration-resistant prostate cancer growth. EMBO J. 2011;30(12):2405-19.
43. Garnis C, Coe BP, Lam SL, Mac Aulay C, Lam WL. Highresolution array CGH increases heterogeneity tolerance in the analysis of clinical samples. Genomics. 2005;85(6):790-3.
44. Prochownik EV. c-Myc: linking transformation and genomic instability. Curr Mol Med. 2008;8(6):446-58.
45. Troncone G, Guerriero E, Pallante P, Berlingieri MT, Ferraro A, Del Vecchio L, et al. UbcH10 expression in human lymphomas. Histopathology. 2009;54(6):731-40.
46. Cunha IW, Carvalho KC, Martins WK, Marques SM, Muto NH, Falzoni R, et al. Identification of genes associated with local aggressiveness and metastatic behavior in soft tissue tumors. Transl Oncol. 2010;3(1):23-32.
47. Takahashi Y, Ishii Y, Nishida Y, Ikarashi M, Nagata T, Nakamura T, et al. Detection of aberrations of ubiquitin-conjugating enzyme E2C gene (UBE2C) in advanced colon cancer with liver metastases by DNA microarray and two-color FISH. Cancer Genet Cytogenet. 2006;168(1):30-5.
48. Guerriero E, Ferraro A, Desiderio D, Pallante P, Berlingieri MT, Iaccarino A, et al. UbcH10 expression on thyroid fine-needle aspirates. Cancer Cytopathol. 2010;118(3):157-65.
49. Donato G, Iofrida G, Lavano A, Volpentesta G, Signorelli F, Pallante PL, et al. Analysis of UbcH10 expression represents a useful tool for the diagnosis and therapy of astrocytic tumors. Clin Neuropathol. 2008;27(4):219-23.
50. Karadag YS, Karadag O, Cicekli E, Ozturk S, Kiraz S, Ozbakir S, et al. Severity of carpal tunnel syndrome assessed with high frequency ultrasonography. Rheumatol Int. 2010;30(6):761-5.
51. Campone M, Campion L, Roche H, Gouraud W, Charbonnel C, Magrangeas F, et al. Prediction of metastatic relapse in nodepositive breast cancer: establishment of a clinicogenomic model after FEC100 adjuvant regimen. Breast Cancer Res Treat. 2008;109(3):491-501.
52. Taylor KJ, Sims AH, Liang L, Faratian D, Muir M, Walker G, et al. Dynamic changes in gene expression in vivo predict prognosis of tamoxifen-treated patients with breast cancer. Breast Cancer Res. 2010;12(3):R39.
53. Wang H, Zhang C, Rorick A, Wu D, Chiu M, Thomas-Ahner J, et al. CCI-779 inhibits cell-cycle G2-M progression and invasion of castration-resistant prostate cancer via attenuation of UBE2C transcription and mRNA stability. Cancer Res. 2011;71(14):4866-76.
54. Zirn B, Samans B, Spangenberg C, Graf N, Eilers M, Gessler M. All-trans retinoic acid treatment of Wilms tumor cells reverses expression of genes associated with high risk and relapse in vivo. Oncogene. 2005;24(33):5246-51.
55. Bavi P, Uddin S, Ahmed M, Jehan Z, Bu R, Abubaker J, et al. Bortezomib stabilizes mitotic cyclins and prevents cell cycle progression via inhibition of UBE2C in colorectal carcinoma. Am J Pathol. 2011;178(5):2109-20.
56. Lee EA, Keutmann MK, Dowling ML, Harris E, Chan G, Kao GD. Inactivation of the mitotic checkpoint as a determinant of the efficacy of microtubule-targeted drugs in killing human cancer cells. Mol Cancer Ther. 2004;3(6):661-9.
57. Laurell C, Velazquez-Fernandez D, Lindsten K, Juhlin C, Enberg U, Geli J, et al. Transcriptional profiling enables molecular classification of adrenocortical tumours. Eur J Endocrinol. 2009;161(1):141-52.
58. Fevre-Montange M, Champier J, Durand A, Wierinckx A, Honnorat J, Guyotat J, et al. Microarray gene expression profiling in meningiomas: differential expression according to grade or histopathological subtype. Int J Oncol. 2009;35(6):1395-407.
59. Bredel M, Bredel C, Juric D, Harsh GR, Vogel H, Recht LD, et al. Functional network analysis reveals extended gliomagenesis pathway maps and three novel MYC-interacting genes in human gliomas. Cancer Res. 2005;65(19):8679-89.
60. Kamalakaran S, Varadan V, Giercksky Russnes HE, Levy D, Kendall J, Janevski A, et al. DNA methylation patterns in luminal breast cancers differ from non-luminal subtypes and can identify relapse risk independent of other clinical variables. Mol Oncol. 2011;5(1):77-92.
61. Parris TZ, Danielsson A, Nemes S, Kovacs A, Delle U, Fallenius G, et al. Clinical implications of gene dosage and gene expression patterns in diploid breast carcinoma. Clin Cancer Res. 2010;16(15):3860-74.
62. Chen CC, Chang TW, Chen FM, Hou MF, Hung SY, Chong IW, et al. Combination of multiple mRNA markers (PTTG1, Survivin, UbcH10 and TK1) in the diagnosis of Taiwanese patients with breast cancer by membrane array. Oncology. 2006;70(6):438-46.
63. Rajkumar T, Sabitha K, Vijayalakshmi N, Shirley S, Bose MV, Gopal G, et al. Identification and validation of genes involved in cervical tumourigenesis. BMC Cancer. 2011;11:80.
64. Narayan G, Bourdon V, Chaganti S, Arias-Pulido H, Nandula SV, Rao PH, et al. Gene dosage alterations revealed by cDNA microarray analysis in cervical cancer: identification of candidate amplified and overexpressed genes. Genes Chromosomes Cancer. 2007;46(4):373-84.
65. Sheffer M, Bacolod MD, Zuk O, Giardina SF, Pincas H, Barany F, et al. Association of survival and disease progression with chromosomal instability: a genomic exploration of colorectal cancer. Proc Natl Acad Sci USA. 2009;106(17):7131-6.
66. Lin J, Raoof DA, Wang Z, Lin MY, Thomas DG, Greenson JK, et al. Expression and effect of inhibition of the ubiquitin-conjugating enzyme E2C on esophageal adenocarcinoma. Neoplasia. 2006;8(12):1062-71.
67. Kadara H, Lacroix L, Behrens C, Solis L, Gu X, Lee JJ, et al. Identification of gene signatures and molecular markers for human lung cancer prognosis using an in vitro lung carcinogenesis system. Cancer Prev Res (Phila). 2009;2(8):702-11.
68. Lee JJ, Au AY, Foukakis T, Barbaro M, Kiss N, Clifton-Bligh R, et al. Array-CGH identifies cyclin D1 and UBCH10 amplicons in anaplastic thyroid carcinoma. Endocr Relat Cancer. 2008;15(3):801-15.