De-acetylation and degradation of HSPA5 is critical for E1A metastasis suppression in breast cancer cells

Oncotarget

Volumn 5, Issue 21, 2014, Pages 10558-10570

  Chang, Yi Wen ^a   Chen, Hsin An ^b,c   Tseng, Chi Feng ^a,d   Hong, Chih Chen ^a   Ma, Jui Ti ^a,d   Hung, Mien Chie ^e,f,g,h   Wu, Chih Hsiung ^b,c   Huang, Ming Te ^b,c   Su, Jen Liang ^a,e,f,g  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^e CHINA MEDICAL UNIVERSITY   (Taiwan)

^f CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^g ASIA UNIVERSITY   (Taiwan)

^h UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Acetylation; Adenovirus type 5 E1A; HSPA5 GRP78 Bip; Metastasis; Ubiquitination

Indexed keywords

E1A ASSOCIATED P300 PROTEIN; E1A PROTEIN; GP78 PROTEIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 5; PROTEASOME; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; EP300 PROTEIN, HUMAN; MESSENGER RNA; MOLECULAR CHAPERONE GRP78; PROTEIN BINDING;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER GENE THERAPY; CELL INVASION ASSAY; CELL MIGRATION ASSAY; CONTROLLED STUDY; DEACETYLATION; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN ADENOVIRUS 5; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; METASTASIS INHIBITION; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; UBIQUITINATION; WESTERN BLOTTING; ACETYLATION; ANIMAL; APOPTOSIS; BREAST NEOPLASMS; CELL MOTION; CELL PROLIFERATION; DRUG SCREENING; ENZYME IMMUNOASSAY; GENETICS; LUNG NEOPLASMS; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; SECONDARY; TUMOR CELL CULTURE;

ACETYLATION; ADENOVIRUS E1A PROTEINS; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; E1A-ASSOCIATED P300 PROTEIN; FEMALE; HEAT-SHOCK PROTEINS; HUMANS; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; LUNG NEOPLASMS; MICE; MICE, SCID; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED; UBIQUITINATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84916930702     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2510     Document Type: Article

References (50)

1. Siegel R, Naishadham D and Jemal A. Cancer statistics, 2013. CA: a cancer journal for clinicians. 2013; 63(1):11-30.
2. Chalasani P, Downey L and Stopeck AT. Caring for the breast cancer survivor: a guide for primary care physicians. The American journal of medicine. 2010; 123(6):489-495.
3. Ma Y and Hendershot LM. The role of the unfolded protein response in tumour development: friend or foe? Nature reviews Cancer. 2004; 4(12):966-977.
4. Lee AS. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem Sci. 2001; 26(8):504-510.
5. Ni M and Lee AS. ER chaperones in mammalian development and human diseases. FEBS Lett. 2007; 581(19):3641-3651.
6. Wang Q, He Z, Zhang J, Wang Y, Wang T, Tong S, Wang L, Wang S and Chen Y. Overexpression of endoplasmic reticulum molecular chaperone GRP94 and GRP78 in human lung cancer tissues and its significance. Cancer Detect Prev. 2005; 29(6):544-551.
7. Fernandez PM, Tabbara SO, Jacobs LK, Manning FC, Tsangaris TN, Schwartz AM, Kennedy KA and Patierno SR. Overexpression of the glucose-regulated stress gene GRP78 in malignant but not benign human breast lesions. Breast cancer research and treatment. 2000; 59(1):15-26.
8. Gazit G, Lu J and Lee AS. De-regulation of GRP stress protein expression in human breast cancer cell lines. Breast cancer research and treatment. 1999; 54(2):135-146.
9. Pootrakul L, Datar RH, Shi SR, Cai J, Hawes D, Groshen SG, Lee AS and Cote RJ. Expression of stress response protein Grp78 is associated with the development of castration-resistant prostate cancer. Clin Cancer Res. 2006; 12(20 Pt 1):5987-5993.
10. Xing X, Lai M, Wang Y, Xu E and Huang Q. Overexpression of glucose-regulated protein 78 in colon cancer. Clin Chim Acta. 2006; 364(1-2):308-315.
11. Zhang J, Jiang Y, Jia Z, Li Q, Gong W, Wang L, Wei D, Yao J, Fang S and Xie K. Association of elevated GRP78 expression with increased lymph node metastasis and poor prognosis in patients with gastric cancer. Clin Exp Metastasis. 2006; 23(7-8):401-410.
12. Shuda M, Kondoh N, Imazeki N, Tanaka K, Okada T, Mori K, Hada A, Arai M, Wakatsuki T, Matsubara O, Yamamoto N and Yamamoto M. Activation of the ATF6, XBP1 and grp78 genes in human hepatocellular carcinoma: a possible involvement of the ER stress pathway in hepatocarcinogenesis. J Hepatol. 2003; 38(5):605-614.
13. Dong D, Stapleton C, Luo B, Xiong S, Ye W, Zhang Y, Jhaveri N, Zhu G, Ye R, Liu Z, Bruhn KW, Craft N, Groshen S, Hofman FM and Lee AS. A critical role for GRP78/BiP in the tumor microenvironment for neovascularization during tumor growth and metastasis. Cancer Res. 2011; 71(8):2848-2857.
14. Fu Y and Lee AS. Glucose regulated proteins in cancer progression, drug resistance and immunotherapy. Cancer Biol Ther. 2006; 5(7):741-744.
15. Dong D, Ni M, Li J, Xiong S, Ye W, Virrey JJ, Mao C, Ye R, Wang M, Pen L, Dubeau L, Groshen S, Hofman FM and Lee AS. Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival, and tumor angiogenesis in transgene-induced mammary tumor development. Cancer Res. 2008; 68(2):498-505.
16. Hortobagyi GN, Hung MC and Lopez-Berestein G. A Phase I multicenter study of E1A gene therapy for patients with metastatic breast cancer and epithelial ovarian cancer that overexpresses HER-2/neu or epithelial ovarian cancer. Hum Gene Ther. 1998; 9(12):1775-1798.
17. Hortobagyi GN, Ueno NT, Xia W, Zhang S, Wolf JK, Putnam JB, Weiden PL, Willey JS, Carey M, Branham DL, Payne JY, Tucker SD, Bartholomeusz C, Kilbourn RG, De Jager RL, Sneige N, et al. Cationic liposome-mediated E1A gene transfer to human breast and ovarian cancer cells and its biologic effects: a phase I clinical trial. J Clin Oncol. 2001; 19(14):3422-3433.
18. Madhusudan S, Tamir A, Bates N, Flanagan E, Gore ME, Barton DP, Harper P, Seckl M, Thomas H, Lemoine NR, Charnock M, Habib NA, Lechler R, Nicholls J, Pignatelli M and Ganesan TS. A multicenter Phase I gene therapy clinical trial involving intraperitoneal administration of E1A-lipid complex in patients with recurrent epithelial ovarian cancer overexpressing HER-2/neu oncogene. Clin Cancer Res. 2004; 10(9):2986-2996.
19. Villaret D, Glisson B, Kenady D, Hanna E, Carey M, Gleich L, Yoo GH, Futran N, Hung MC, Anklesaria P and Heald AE. A multicenter phase II study of tgDCC-E1A for the intratumoral treatment of patients with recurrent head and neck squamous cell carcinoma. Head Neck. 2002; 24(7):661-669.
20. Yu D, Wolf JK, Scanlon M, Price JE and Hung MC. Enhanced c-erbB-2/neu expression in human ovarian cancer cells correlates with more severe malignancy that can be suppressed by E1A. Cancer Res. 1993; 53(4):891-898.
21. Ueno NT, Yu D and Hung MC. Chemosensitization of HER-2/neu-overexpressing human breast cancer cells to paclitaxel (Taxol) by adenovirus type 5 E1A. Oncogene. 1997; 15(8):953-960.
22. Liao Y and Hung MC. Regulation of the activity of p38 mitogen-activated protein kinase by Akt in cancer and adenoviral protein E1A-mediated sensitization to apoptosis. Molecular and cellular biology. 2003; 23(19):6836-6848.
23. Shao R, Tsai EM, Wei K, von Lindern R, Chen YH, Makino K and Hung MC. E1A inhibition of radiation-induced NFkappaB activity through suppression of IKK activity and IkappaB degradation, independent of Akt activation. Cancer Res. 2001; 61(20):7413-7416.
24. Su JL, Chen PB, Chen YH, Chen SC, Chang YW, Jan YH, Cheng X, Hsiao M and Hung MC. Downregulation of microRNA miR-520h by E1A contributes to anticancer activity. Cancer Res. 2010; 70(12):5096-5108.
25. Grooteclaes ML and Frisch SM. Evidence for a function of CtBP in epithelial gene regulation and anoikis. Oncogene. 2000; 19(33):3823-3828.
26. Su JL, Cheng XY, Yamaguchi H, Chang YW, Hou CF, Lee DF, Ko HW, Hua KT, Wang YN, Hsiao M, Chen PSB, Hsu JM, Bast RC, Hortobagyi GN and Hung MC. FOXO3a-Dependent Mechanism of E1A-Induced Chemosensitization. Cancer Res. 2011; 71(21):6878-6887.
27. Chen B, Mariano J, Tsai YC, Chan AH, Cohen M and Weissman AM. The activity of a human endoplasmic reticulum-associated degradation E3, gp78, requires its Cue domain, RING finger, and an E2-binding site. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103(2):341-346.
28. Cyr DM, Hohfeld J and Patterson C. Protein quality control: U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem Sci. 2002; 27(7):368-375.
29. Soucy TA, Smith PG and Rolfe M. Targeting NEDD8-activated cullin-RING ligases for the treatment of cancer. Clin Cancer Res. 2009; 15(12):3912-3916.
30. Takahashi R, Imai Y, Hattori N and Mizuno Y. Parkin and endoplasmic reticulum stress. Ann N Y Acad Sci. 2003; 991:101-106.
31. Rao R, Nalluri S, Kolhe R, Yang Y, Fiskus W, Chen J, Ha K, Buckley KM, Balusu R, Coothankandaswamy V, Joshi A, Atadja P and Bhalla KN. Treatment with panobinostat induces glucose-regulated protein 78 acetylation and endoplasmic reticulum stress in breast cancer cells. Mol Cancer Ther. 2010; 9(4):942-952.
32. Caron C, Boyault C and Khochbin S. Regulatory cross-talk between lysine acetylation and ubiquitination: role in the control of protein stability. Bioessays. 2005; 27(4):408-415.
33. Jin YH, Jeon EJ, Li QL, Lee YH, Choi JK, Kim WJ, Lee KY and Bae SC. Transforming growth factor-beta stimulates p300-dependent RUNX3 acetylation, which inhibits ubiquitination-mediated degradation. The Journal of biological chemistry. 2004; 279(28):29409-29417.
34. Horwitz GA, Zhang K, McBrian MA, Grunstein M, Kurdistani SK and Berk AJ. Adenovirus small e1a alters global patterns of histone modification. Science. 2008; 321(5892):1084-1085.
35. Lee AS. Glucose-regulated proteins in cancer: molecular mechanisms and therapeutic potential. Nature reviews Cancer. 2014; 14(4):263-276.
36. Luo B and Lee AS. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene. 2013; 32(7):805-818.
37. Fu Y, Wey S, Wang M, Ye R, Liao CP, Roy-Burman P and Lee AS. Pten null prostate tumorigenesis and AKT activation are blocked by targeted knockout of ER chaperone GRP78/BiP in prostate epithelium. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(49):19444-19449.
38. Chiu CC, Lin CY, Lee LY, Chen YJ, Kuo TF, Chang JT, Liao CT, Wang HM, Yen TC, Shen CR, Liao SK and Cheng AJ. Glucose-regulated protein 78 regulates multiple malignant phenotypes in head and neck cancer and may serve as a molecular target of therapeutic intervention. Mol Cancer Ther. 2008; 7(9):2788-2797.
39. Su R, Li Z, Li H, Song H, Bao C, Wei J and Cheng L. Grp78 promotes the invasion of hepatocellular carcinoma. BMC cancer. 2010; 10:20.
40. Misra UK, Deedwania R and Pizzo SV. Binding of activated alpha2-macroglobulin to its cell surface receptor GRP78 in 1-LN prostate cancer cells regulates PAK-2-dependent activation of LIMK. The Journal of biological chemistry. 2005; 280(28):26278-26286.
41. Li Z, Zhang L, Li H, Shan S and Li Z. Glucose regulated protein 78 promotes cell invasion via regulation of uPA production and secretion in colon cancer cells. BMB reports. 2014; 47(8):445-450.
42. Mollapour M, Tsutsumi S, Truman AW, Xu W, Vaughan CK, Beebe K, Konstantinova A, Vourganti S, Panaretou B, Piper PW, Trepel JB, Prodromou C, Pearl LH and Neckers L. Threonine 22 phosphorylation attenuates Hsp90 interaction with cochaperones and affects its chaperone activity. Molecular cell. 2011; 41(6):672-681.
43. Yang Y, Rao R, Shen J, Tang Y, Fiskus W, Nechtman J, Atadja P and Bhalla K. Role of acetylation and extracellular location of heat shock protein 90alpha in tumor cell invasion. Cancer Res. 2008; 68(12):4833-4842.
44. Grossman SR, Deato ME, Brignone C, Chan HM, Kung AL, Tagami H, Nakatani Y and Livingston DM. Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science. 2003; 300(5617):342-344.
45. Brooks CL, Li M and Gu W. Monoubiquitination: the signal for p53 nuclear export? Cell Cycle. 2004; 3(4):436-438.
46. Ni M, Zhang Y and Lee AS. Beyond the endoplasmic reticulum: atypical GRP78 in cell viability, signalling and therapeutic targeting. Biochem J. 2011; 434(2):181-188.
47. Wang Y, Guan S, Acharya P, Liu Y, Thirumaran RK, Brandman R, Schuetz EG, Burlingame AL and Correia MA. Multisite phosphorylation of human liver cytochrome P450 3A4 enhances Its gp78-and CHIP-mediated ubiquitination: a pivotal role of its Ser-478 residue in the gp78-catalyzed reaction. Mol Cell Proteomics. 2012; 11(2):M111 010132.
48. Gordon V and Banerji S. Molecular pathways: PI3K pathway targets in triple-negative breast cancers. Clin Cancer Res. 2013; 19(14):3738-3744.
49. Xie X HJ, Choi MG, Xia W, Yamaguchi H, Chen CT, Trinh BQ, Lu Z, Ueno NT, Wolf JK, Bast RC Jr, Hung MC. A novel hTERT promoter-driven E1A therapeutic for ovarian cancer. Mol Cancer Ther. 2009; 8(8):2375-2382.
50. O'Connor MJ, Zimmermann H, Nielsen S, Bernard HU and Kouzarides T. Characterization of an E1A-CBP interaction defines a novel transcriptional adapter motif (TRAM) in CBP/p300. Journal of virology. 1999; 73(5):3574-3581.