NRAGE promotes cell proliferation by stabilizing PCNA in a ubiquitin-proteasome pathway in esophageal carcinomas

Carcinogenesis

Volumn 35, Issue 7, 2014, Pages

  Yang, Qingyuan ^a   Ou, Chao ^b   Liu, Mei ^c   Xiao, Weifan ^a   Wen, Chuanjun ^c   Sun, Fenyong ^a  

^a TENTH PEOPLE S HOSPITAL OF TONGJI UNIVERSITY   (China)

^b GUANGXI MEDICAL UNIVERSITY   (China)

^c NANJING NORMAL UNIVERSITY   (China)

Author keywords

Cell growth; NRAGE; PCNA; Polyubiquitylation; Proteasome degradation; USP10

Indexed keywords

CYCLINE; DEUBIQUITINASE; DNA DIRECTED DNA POLYMERASE GAMMA; MESSENGER RNA; ONCOPROTEIN; PROTEASOME; PROTEIN; PROTEIN NRAGE; UBIQUITIN; UBIQUITIN SPECIFIC PROTEASE 10; UNCLASSIFIED DRUG; MAGED1 PROTEIN, HUMAN; SMALL INTERFERING RNA; TUMOR ANTIGEN; TUMOR PROTEIN; UBIQUITIN THIOLESTERASE; USP10 PROTEIN, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CANCER TISSUE; CARCINOGENESIS; CELL CYCLE S PHASE; CELL LYSATE; CELL PROLIFERATION; COLONY FORMATION; COMPARATIVE STUDY; CONTROLLED STUDY; ESOPHAGUS CARCINOMA; FEEDBACK SYSTEM; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; GENE SILENCING; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MALE; METASTASIS; MOUSE; MTT ASSAY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UBIQUITINATION; ANIMAL; CANCER STAGING; COHORT ANALYSIS; DRUG ANTAGONISM; DRUG SCREENING; ENZYME IMMUNOASSAY; ESOPHAGUS; ESOPHAGUS TUMOR; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; LYMPH NODE METASTASIS; METABOLISM; MIDDLE AGED; NUDE MOUSE; PATHOLOGY; PROTEIN DEGRADATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SQUAMOUS CELL CARCINOMA; TISSUE MICROARRAY; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; ANTIGENS, NEOPLASM; BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL PROLIFERATION; COHORT STUDIES; ESOPHAGEAL NEOPLASMS; ESOPHAGUS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; LYMPHATIC METASTASIS; MALE; MICE; MICE, NUDE; MIDDLE AGED; NEOPLASM PROTEINS; NEOPLASM STAGING; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TISSUE ARRAY ANALYSIS; TUMOR CELLS, CULTURED; UBIQUITIN THIOLESTERASE; UBIQUITINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84904018869     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgu084     Document Type: Article

References (42)

1. Sun, J.M., et al., Interleukin 10 rs1800872 T> G Polymorphism was Associated with an Increased Risk of Esophageal Cancer in a Chinese Population. Asian Pac J Cancer Prev, 2013. 14(6): p. 3443-7.
2. Pickens, A. and M.B. Orringer, Geographical distribution and racial disparity in esophageal cancer. Ann Thorac Surg, 2003. 76(4): p. S1367-9.
3. Xu, X., et al., An association study on genetic polymorphisms of Rab37 gene with the risk of esophageal squamous cell carcinoma in a Chinese Han population. Int J Med Sci, 2013. 10(3): p. 235-42.
4. Masuda, Y., et al., Dlxin-1, a novel protein that binds Dlx5 and regulates its transcriptional function. J Biol Chem, 2001. 276(7): p. 5331-8.
5. Di Certo, M.G., et al., NRAGE associates with the anti-apoptotic factor Che-1 and regulates its degradation to induce cell death. J Cell Sci, 2007. 120(Pt 11): p. 1852-8.
6. Salehi, A.H., S. Xanthoudakis, and P.A. Barker, NRAGE, a p75 neurotrophin receptor-interacting protein, induces caspase activation and cell death through a JNK-dependent mitochondrial pathway. J Biol Chem, 2002. 277(50): p. 48043-50.
7. Williams, M.E., et al., UNC5H1 induces apoptosis via its juxtamembrane region through an interaction with NRAGE. J Biol Chem, 2003. 278(19): p. 17483-90.
8. Matluk, N., et al., A role for NRAGE in NF-kappaB activation through the non-canonical BMP pathway. BMC Biol, 2010. 8: p. 7.
9. Matsuda, T., et al., The receptor tyrosine kinase Ror2 associates with the melanoma-associated antigen (MAGE) family protein Dlxin-1 and regulates its intracellular distribution. J Biol Chem, 2003. 278(31): p. 29057-64.
10. Sasaki, A., et al., A RING finger protein Praja1 regulates Dlx5-dependent transcription through its ubiquitin ligase activity for the Dlx/Msx-interacting MAGE/Necdin family protein, Dlxin-1. J Biol Chem, 2002. 277(25): p. 22541-6.
11. Friedberg, E.C., Reversible monoubiquitination of PCNA: A novel slant on regulating translesion DNA synthesis. Mol Cell, 2006. 22(2): p. 150-2.
12. Peng, J., et al., A proteomics approach to understanding protein ubiquitination. Nat Biotechnol, 2003. 21(8): p. 921-6.
13. Al-Hakim, A., et al., The ubiquitous role of ubiquitin in the DNA damage response. DNA Repair (Amst), 2010. 9(12): p. 1229-40.
14. Fox, J.T., K.Y. Lee, and K. Myung, Dynamic regulation of PCNA ubiquitylation/deubiquitylation. FEBS Lett, 2011. 585(18): p. 2780-5.
15. Chen, J., W. Bozza, and Z. Zhuang, Ubiquitination of PCNA and its essential role in eukaryotic translesion synthesis. Cell Biochem Biophys, 2011. 60(1-2): p. 47-60.
16. Moldovan, G.L., B. Pfander, and S. Jentsch, PCNA, the maestro of the replication fork. Cell, 2007. 129(4): p. 665-79.
17. Ulrich, H.D., Regulating post-translational modifications of the eukaryotic replication clamp PCNA. DNA Repair (Amst), 2009. 8(4): p. 461-9.
18. Wen, C.J., et al., hNRAGE, a human neurotrophin receptor interacting MAGE homologue, regulates p53 transcriptional activity and inhibits cell proliferation. FEBS Lett, 2004. 564(1-2): p. 171-6.
19. Kumar, S., et al., A pathway for the control of anoikis sensitivity by E-cadherin and epithelial-to-mesenchymal transition. Mol Cell Biol, 2011. 31(19): p. 4036-51.
20. Wu, W., et al., Antitumor activity of folate-targeted, paclitaxel-loaded polymeric micelles on a human esophageal EC9706 cancer cell line. Int J Nanomedicine, 2012. 7: p. 3487-502.
21. Emerson, J.W., et al., Quantitative assessment of tissue biomarkers and construction of a model to predict outcome in breast cancer using multiple imputation. Cancer Inform, 2009. 7: p. 29-40.
22. Zimpfer, A., et al., Construction and validation of a bone marrow tissue microarray. J Clin Pathol, 2007. 60(1): p. 57-61.
23. Oconnell, M.J., C. Norbury, and P. Nurse, Premature Chromatin Condensation Upon Accumulation of Nima. Embo Journal, 1994. 13(20): p. 4926-4937.
24. Li, J.K., A.N. Meyer, and D.J. Donoghue, Requirement for Phosphorylation of Cyclin B1 for Xenopus Oocyte Maturation. Molecular Biology of the Cell, 1995. 6(9): p. 1111-1124.
25. Toyoshima-Morimoto, F., E. Taniguchi, and E. Nishida, Plk1 promotes nuclear translocation of human Cdc25C during prophase. Embo Reports, 2002. 3(4): p. 341-348.
26. Bologna-Molina, R., et al., Comparison of the value of PCNA and Ki-67 as markers of cell proliferation in ameloblastic tumors. Med Oral Patol Oral Cir Bucal, 2013. 18(2): p. e174-9.
27. Chaloob, M.K., et al., Immunohistochemical Expression of Ki-67, PCNA and CD34 in Astrocytomas: A Clinicopathological Study. Oman Med J, 2012. 27(5): p. 368-74.
28. Tan, Z., et al., Small-molecule targeting of proliferating cell nuclear antigen chromatin association inhibits tumor cell growth. Mol Pharmacol, 2012. 81(6): p. 811-9.
29. Mallette, F.A. and S. Richard, K48-linked ubiquitination and protein degradation regulate 53BP1 recruitment at DNA damage sites. Cell Res, 2012. 22(8): p. 1221-3.
30. Yuan, J., et al., USP10 regulates p53 localization and stability by deubiquitinating p53. Cell, 2010. 140(3): p. 384-96.
31. Bertrand, M.J., et al., NRAGE, a p75NTR adaptor protein, is required for developmental apoptosis in vivo. Cell Death Differ, 2008. 15(12): p. 1921-9.
32. Tian, X.X., et al., BRCA2 suppresses cell proliferation via stabilizing MAGE-D1. Cancer Res, 2005. 65(11): p. 4747-53.
33. Kuwajima, T., et al., Necdin interacts with the Msx2 homeodomain protein via MAGE-D1 to promote myogenic differentiation of C2C12 cells. J Biol Chem, 2004. 279(39): p. 40484-93.
34. Wang, F., et al., Salinomycin inhibits proliferation and induces apoptosis of human hepatocellular carcinoma cells in vitro and in vivo. PLoS One, 2012. 7(12): p. e50638.
35. Kendall, S.E., et al., Expression analysis of a novel p75(NTR) signaling protein, which regulates cell cycle progression and apoptosis. Mech Dev, 2002. 117(1-2): p. 187-200.
36. Pold, M., et al., Identification of a new, unorthodox member of the MAGE gene family. Genomics, 1999. 59(2): p. 161-7.
37. Lucas, S., F. Brasseur, and T. Boon, A new MAGE gene with ubiquitous expression does not code for known MAGE antigens recognized by T cells. Cancer Res, 1999. 59(16): p. 4100-3.
38. Mouri, A., et al., MAGE-D1 regulates expression of depression-like behavior through serotonin transporter ubiquitylation. J Neurosci, 2012. 32(13): p. 4562-80.
39. Doyle, J.M., et al., MAGE-RING protein complexes comprise a family of E3 ubiquitin ligases. Mol Cell, 2010. 39(6): p. 963-74.
40. Burkovics, P., et al., Role of PCNA-dependent stimulation of 3'-phosphodiesterase and 3'-5' exonuclease activities of human Ape2 in repair of oxidative DNA damage. Nucleic Acids Res, 2009. 37(13): p. 4247-55.
41. Zlatanou, A., et al., The hMsh2-hMsh6 complex acts in concert with monoubiquitinated PCNA and Pol eta in response to oxidative DNA damage in human cells. Mol Cell, 2011. 43(4): p. 649-62.
42. Xue, X.Y., et al., Relationship between NRAGE and the radioresistance of esophageal carcinoma cell line TE13R120. Chin J Cancer, 2010. 29(10): p. 900-6.