Nuclear Localization of DNAJB6 Is Associated with Survival of Patients with Esophageal Cancer and Reduces AKT Signaling and Proliferation of Cancer Cells

Gastroenterology

Volumn 149, Issue 7, 2015, Pages 1825-1836.e5

  Yu, Valen Zhuoyou ^a   Wong, Victor Chun Lam ^a   Dai, Wei ^a   Ko, Josephine Mun Yee ^a   Lam, Alfred King Yin ^b   Chan, Kwok Wah ^a   Samant, Rajeev S ^c   Lung, Hong Lok ^a   Shuen, Wai Ho ^a   Law, Simon ^a   Chan, Yuen Piu ^a   Lee, Nikki Pui Yue ^a   Tong, Daniel King Hung ^a   Law, Tsz Ting ^a   Lee, Victor Ho Fun ^a   Lung, Maria Li ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b GRIFFITH UNIVERSITY   (Australia)

^c University of Alabama at Birmingham   (United States)

Author keywords

Prognostic Marker; Signal Transduction; Tissue Microarray; Tumor Suppressor

Indexed keywords

DNAJB6 PROTEIN; PROTEIN DNAJ; PROTEIN KINASE B; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; AKT1 PROTEIN, HUMAN; CHAPERONE; DNAJB6 PROTEIN, HUMAN; HEAT SHOCK PROTEIN 40; NERVE PROTEIN; PROTEIN KINASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER CELL; CANCER CELL LINE; CANCER LOCALIZATION; CANCER MORTALITY; CELL PROLIFERATION; COHORT ANALYSIS; CONTROLLED STUDY; EPITHELIUM CELL; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS RESECTION; FEMALE; FLUORESCENCE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMORTALIZED CELL LINE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN INTERACTION; RETROSPECTIVE STUDY; RISK FACTOR; SIGNAL TRANSDUCTION; SURVIVAL RATE; SURVIVAL TIME; TUMOR XENOGRAFT; WILD TYPE; ACTIVE TRANSPORT; AGED; ANIMAL; ANTAGONISTS AND INHIBITORS; CARCINOMA, SQUAMOUS CELL; CELL NUCLEUS; DRUG EFFECTS; ENZYMOLOGY; ESOPHAGEAL NEOPLASMS; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; KAPLAN MEIER METHOD; MALE; METABOLISM; MIDDLE AGED; MORTALITY; MUTATION; NUDE MOUSE; PATHOLOGY; PROPORTIONAL HAZARDS MODEL; RNA INTERFERENCE; TIME; TREATMENT OUTCOME; TUMOR CELL LINE; XENOGRAFT;

ACTIVE TRANSPORT, CELL NUCLEUS; AGED; ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL NUCLEUS; CELL PROLIFERATION; ESOPHAGEAL NEOPLASMS; ESOPHAGECTOMY; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HETEROGRAFTS; HSP40 HEAT-SHOCK PROTEINS; HUMANS; KAPLAN-MEIER ESTIMATE; LYMPHATIC METASTASIS; MALE; MICE, NUDE; MIDDLE AGED; MOLECULAR CHAPERONES; MUTATION; NERVE TISSUE PROTEINS; PROPORTIONAL HAZARDS MODELS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RETROSPECTIVE STUDIES; RISK FACTORS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TREATMENT OUTCOME;

EID: 84952983430     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2015.08.025     Document Type: Article

References (58)

1. J. Ferlay, I. Soerjomataram, R. Dikshit, and et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012 Int J Cancer 136 2015 E359 E386
2. H.Z. Zhang, G.F. Jin, and H.B. Shen Epidemiologic differences in esophageal cancer between Asian and Western populations Chin J Cancer 31 2012 281 286
3. R. Hanai, and K. Mashima Characterization of two isoforms of a human DnaJ homologue, HSJ2 Mol Biol Rep 30 2003 149 153
4. J. Sarparanta, P.H. Jonson, C. Golzio, and et al. Mutations affecting the cytoplasmic functions of the co-chaperone DNAJB6 cause limb-girdle muscular dystrophy Nat Genet 44 2012 450 455 S1-S2
5. A. Mitra, R.A. Fillmore, B.J. Metge, and et al. Large isoform of MRJ (DNAJB6) reduces malignant activity of breast cancer Breast Cancer Res 10 2008 R22
6. A. Mitra, M.E. Menezes, L.A. Shevde, and et al. DNAJB6 induces degradation of beta-catenin and causes partial reversal of mesenchymal phenotype J Biol Chem 285 2010 24686 24694
7. A. Mitra, M.E. Menezes, L.K. Pannell, and et al. DNAJB6 chaperones PP2A mediated dephosphorylation of GSK3beta to downregulate beta-catenin transcription target, osteopontin Oncogene 31 2012 4472 4483
8. D.P. Ding, Z.L. Chen, X.H. Zhao, and et al. miR-29c induces cell cycle arrest in esophageal squamous cell carcinoma by modulating cyclin E expression Carcinogenesis 32 2011 1025 1032
9. J. Liang, J. Zubovitz, T. Petrocelli, and et al. PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest Nat Med 8 2002 1153 1160
10. G. Viglietto, M.L. Motti, P. Bruni, and et al. Cytoplasmic relocalization and inhibition of the cyclin-dependent kinase inhibitor p27(Kip1) by PKB/Akt-mediated phosphorylation in breast cancer Nat Med 8 2002 1136 1144
11. B.B. Aggarwal, S. Banerjee, U. Bharadwaj, and et al. Curcumin induces the degradation of cyclin E expression through ubiquitin-dependent pathway and up-regulates cyclin-dependent kinase inhibitors p21 and p27 in multiple human tumor cell lines Biochem Pharmacol 73 2007 1024 1032
12. J. Bloom, and M. Pagano Deregulated degradation of the cdk inhibitor p27 and malignant transformation Semin Cancer Biol 13 2003 41 47
13. P.D. Hsu, E.S. Lander, and F. Zhang Development and applications of CRISPR-Cas9 for genome engineering Cell 157 2014 1262 1278
14. M. Andjelkovic, T. Jakubowicz, P. Cron, and et al. Activation and phosphorylation of a pleckstrin homology domain containing protein kinase (RAC-PK/PKB) promoted by serum and protein phosphatase inhibitors Proc Natl Acad Sci U S A 93 1996 5699 5704
15. S. Ugi, T. Imamura, H. Maegawa, and et al. Protein phosphatase 2A negatively regulates insulin's metabolic signaling pathway by inhibiting Akt (protein kinase B) activity in 3T3-L1 adipocytes Mol Cell Biol 24 2004 8778 8789
16. G.S. Filonov, and V.V. Verkhusha A near-infrared BiFC reporter for in vivo imaging of protein-protein interactions Chem Biol 20 2013 1078 1086
17. I. Vivanco, and C.L. Sawyers The phosphatidylinositol 3-kinase AKT pathway in human cancer Nat Rev Cancer 2 2002 489 501
18. M.P. Scheid, and J.R. Woodgett Unravelling the activation mechanisms of protein kinase B/Akt FEBS Lett 546 2003 108 112
19. D.C. Lin, J.J. Hao, Y. Nagata, and et al. Genomic and molecular characterization of esophageal squamous cell carcinoma Nat Genet 46 2014 467 473
20. D. Wall, M. Zylicz, and C. Georgopoulos The NH2-terminal 108 amino acids of the Escherichia coli DnaJ protein stimulate the ATPase activity of DnaK and are sufficient for lambda replication J Biol Chem 269 1994 5446 5451
21. J. Tsai, and M.G. Douglas A conserved HPD sequence of the J-domain is necessary for YDJ1 stimulation of Hsp70 ATPase activity at a site distinct from substrate binding J Biol Chem 271 1996 9347 9354
22. F. Hennessy, M.E. Cheetham, H.W. Dirr, and et al. Analysis of the levels of conservation of the J domain among the various types of DnaJ-like proteins Cell Stress Chaperones 5 2000 347 358
23. R. Polanowska-Grabowska, C.G. Simon Jr., R. Falchetto, and et al. Platelet adhesion to collagen under flow causes dissociation of a phosphoprotein complex of heat-shock proteins and protein phosphatase 1 Blood 90 1997 1516 1526
24. K.A. Whalen, R. de Jesus, J.A. Kean, and et al. Genetic analysis of the polyomavirus DnaJ domain J Virol 79 2005 9982 9990
25. B. McCright, and D.M. Virshup Identification of a new family of protein phosphatase 2A regulatory subunits J Biol Chem 270 1995 26123 26128
26. T.T. Zhang, Y.Y. Jiang, L. Shang, and et al. Overexpression of DNAJB6 promotes colorectal cancer cell invasion through an IQGAP1/ERK-dependent signaling pathway Mol Carcinog 54 2015 1205 1213
27. D. Uchida, N.M. Begum, Y. Tomizuka, and et al. Acquisition of lymph node, but not distant metastatic potentials, by the overexpression of CXCR4 in human oral squamous cell carcinoma Lab Invest 84 2004 1538 1546
28. H.F. Yuen, Y.P. Chan, K.K. Chan, and et al. Id-1 and Id-2 are markers for metastasis and prognosis in oesophageal squamous cell carcinoma Br J Cancer 97 2007 1409 1415
29. S.H. Chan, J.M. Yee Ko, K.W. Chan, and et al. The ECM protein LTBP-2 is a suppressor of esophageal squamous cell carcinoma tumor formation but higher tumor expression associates with poor patient outcome Int J Cancer 129 2011 565 573
30. A. Salajegheh, E. Dolan-Evans, E. Sullivan, and et al. The expression profiles of the galectin gene family in primary and metastatic papillary thyroid carcinoma with particular emphasis on galectin-1 and galectin-3 expression Exp Mol Pathol 96 2014 212 218
31. H. Zhang, Y. Jin, X. Chen, and et al. Cytogenetic aberrations in immortalization of esophageal epithelial cells Cancer Genet Cytogenet 165 2006 25 35
32. C.P. Hu, H.G. Hsieh, K.Y. Chien, and et al. Biologic properties of three newly established human esophageal carcinoma cell lines J Natl Cancer Inst 72 1984 577 583
33. C.H. Mok, E.C. Chew, D.J. Riches, and et al. Biological characteristics of a newly established human oesophageal carcinoma cell line Anticancer Res 7 1987 409 415
34. Q.Q. Pan Studies on esophageal cancer cells in vitro Proc Chin Acad Med Sci Peking Union Med Coll 4 1989 52 57
35. Y.C. Hu, K.Y. Lam, S.Y. Law, and et al. Establishment, characterization, karyotyping, and comparative genomic hybridization analysis of HKESC-2 and HKESC-3: two newly established human esophageal squamous cell carcinoma cell lines Cancer Genet Cytogenet 135 2002 120 127
36. Y. Shimada, M. Imamura, T. Wagata, and et al. Characterization of 21 newly established esophageal cancer cell lines Cancer 69 1992 277 284
37. J.C. Tang, T.S. Wan, N. Wong, and et al. Establishment and characterization of a new xenograft-derived human esophageal squamous cell carcinoma cell line SLMT-1 of Chinese origin Cancer Genet Cytogenet 124 2001 36 41
38. K.K.H. Takahashi, C.-T. Chan, T. Hosono, and et al. A case of esophageal carcinoma metastatic to the mandible and characterization of two cell lines (T. T and T. Tn) established from the oral tumor Jpn J Oral Maxillofac Surg 36 1990 307 316
39. M. Lieber, B. Smith, A. Szakal, and et al. A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells Int J Cancer 17 1976 62 70
40. W.F. Scherer, J.T. Syverton, and G.O. Gey Studies on the propagation in vitro of poliomyelitis viruses. IV. Viral multiplication in a stable strain of human malignant epithelial cells (strain HeLa) derived from an epidermoid carcinoma of the cervix J Exp Med 97 1953 695 710
41. R. Glaser, H.Y. Zhang, K.T. Yao, and et al. Two epithelial tumor cell lines (HNE-1 and HONE-1) latently infected with Epstein-Barr virus that were derived from nasopharyngeal carcinomas Proc Natl Acad Sci U S A 86 1989 9524 9528
42. A.P. Kyriazis, L. DiPersio, G.J. Michael, and et al. Growth patterns and metastatic behavior of human tumors growing in athymic mice Cancer Res 38 1978 3186 3190
43. P.A. Jones, W.E. Laug, and W.F. Benedict Fibrinolytic activity in a human fibrosarcoma cell line and evidence for the induction of plasminogen activator secretion during tumor formation Cell 6 1975 245 252
44. D.B. Rifkin, J.N. Loeb, G. Moore, and et al. Properties of plasminogen activators formed by neoplastic human cell cultures J Exp Med 139 1974 1317 1328
45. D.C. Rijken, and D. Collen Purification and characterization of the plasminogen activator secreted by human melanoma cells in culture J Biol Chem 256 1981 7035 7041
46. A.L. Schwartz, S.E. Fridovich, B.B. Knowles, and et al. Characterization of the asialoglycoprotein receptor in a continuous hepatoma line J Biol Chem 256 1981 8878 8881
47. H.M. Li, C. Man, Y. Jin, and et al. Molecular and cytogenetic changes involved in the immortalization of nasopharyngeal epithelial cells by telomerase Int J Cancer 119 2006 1567 1576
48. B. Li, S.W. Tsao, K.W. Chan, and et al. Id1-induced IGF-II and its autocrine/endocrine promotion of esophageal cancer progression and chemoresistance-implications for IGF-II and IGF-IR-targeted therapy Clin Cancer Res 20 2014 2651 2662
49. J.M. Ko, P.L. Chan, W.L. Yau, and et al. Monochromosome transfer and microarray analysis identify a critical tumor-suppressive region mapping to chromosome 13q14 and THSD1 in esophageal carcinoma Mol Cancer Res 6 2008 592 603
50. N.A. Kearns, R.M. Genga, M.S. Enuameh, and et al. Cas9 effector-mediated regulation of transcription and differentiation in human pluripotent stem cells Development 141 2014 219 223
51. P.H. Lo, J.M. Ko, Z.Y. Yu, and et al. The LIM domain protein, CRIP2, promotes apoptosis in esophageal squamous cell carcinoma Cancer Lett 316 2012 39 45
52. H.L. Lung, D.K. Bangarusamy, D. Xie, and et al. THY1 is a candidate tumour suppressor gene with decreased expression in metastatic nasopharyngeal carcinoma Oncogene 24 2005 6525 6532
53. H.L. Lung, A.K. Cheung, Y. Cheng, and et al. Functional characterization of THY1 as a tumor suppressor gene with antiinvasive activity in nasopharyngeal carcinoma Int J Cancer 127 2010 304 312
54. A.C. Leung, V.C. Wong, L.C. Yang, and et al. Frequent decreased expression of candidate tumor suppressor gene, DEC1, and its anchorage-independent growth properties and impact on global gene expression in esophageal carcinoma Int J Cancer 122 2008 587 594
55. D.A. Schoenfeld Sample-size formula for the proportional-hazards regression model Biometrics 39 1983 499 503
56. R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from: http://www.R-project.org/. Accessed 2013.
57. Y. Benjamini, and Y. Hochberg Controlling the false discovery rate - a practical and powerful approach to multiple testing J R Stat Soc Series B Methodol 57 1995 289 300
58. A. Bhattacharjee, W.G. Richards, J. Staunton, and et al. Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses Proc Natl Acad Sci U S A 98 2001 13790 13795