Elevated serine protease HtrA1 inhibits cell proliferation, reduces invasion, and induces apoptosis in esophageal squamous cell carcinoma by blocking the nuclear factor-κB signaling pathway

Tumor Biology

Volumn 34, Issue 1, 2013, Pages 317-328

  Xia, Jin ^a   Wang, Feng ^a   Wang, Liuxing ^a   Fan, Qingxia ^a  

^a THE FIRST AFFILIATED HOSPITAL OF ZHENGZHOU UNIVERSITY   (China)

Author keywords

Esophageal squamous cell carcinoma; High temperature requirement protein A1; Nuclear factor B signaling pathway; Serine protease

Indexed keywords

CASPASE 3; CYCLIN D1; GELATINASE B; HIGH TEMPERATURE REQUIREMENT PROTEIN A1; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KI 67 ANTIGEN; MESSENGER RNA; PROTEIN BCL 2; PROTEIN BCL XL; SERINE PROTEINASE; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER STAGING; CARCINOGENESIS; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; ENZYME ACTIVITY; ESOPHAGEAL CELL; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS MUCOSA; FEMALE; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SURVIVAL RATE;

EID: 84872788844     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-012-0553-6     Document Type: Article

References (55)

1. J Zumbrunn B Trueb 1996 Primary structure of a putative serine protease specific for IGF-binding proteins FEBS Lett. 398 2-3 187 192 8977104 10.1016/S0014-5793(96)01229-X 1:CAS:528:DyaK28Xnt1Kru7s%3D
2. J Zumbrunn B Trueb 1997 Localization of the gene for a serine protease with IGF-binding domain (PRSS11) to human chromosome 10q25.3-q26.2 Genomics 45 2 461 462 9344681 10.1006/geno.1997.4953 1:CAS:528:DyaK2sXntVejsrc%3D
3. A Baldi A De Luca M Morini T Battista A Felsani F Baldi, et al. 2002 The HtrA1 serine protease is down-regulated during human melanoma progression and represses growth of metastatic melanoma cells Oncogene 21 43 6684 6688 12242667 10.1038/sj.onc.1205911 1:CAS:528:DC%2BD38XntFenu7Y%3D
4. J Chien J Staub SI Hu MR Erickson-Johnson FJ Couch DI Smith, et al. 2004 A candidate tumor suppressor HtrA1 is downregulated in ovarian cancer Oncogene 23 8 1636 1644 14716297 10.1038/sj.onc.1207271 1:CAS:528:DC%2BD2cXhsFOhtrs%3D
5. J Chien G Aletti A Baldi V Catalano P Muretto GL Keeney, et al. 2006 Serine protease HtrA1 modulates chemotherapy-induced cytotoxicity J Clin Invest. 116 7 1994 2004 16767218 10.1172/JCI27698 1:CAS:528:DC%2BD28XmvV2lurY%3D
6. A De Luca M De Falco L De Luca R Penta V Shridhar F Baldi, et al. 2004 Pattern of expression of HtrA1 during mouse development J Histochem Cytochem. 52 12 1609 1617 15557215 10.1369/jhc.4A6330.2004
7. J Narkiewicz D Klasa-Mazurkiewicz D Zurawa-Janicka J Skorko-Glonek J Emerich B Lipinska 2008 Changes in mRNA and protein levels of human HtrA1, HtrA2 and HtrA3 in ovarian cancer Clin Biochem. 41 7-8 561 569 18241672 10.1016/j.clinbiochem.2008.01.004 1:CAS:528:DC%2BD1cXks12itLY%3D
8. V Esposito M Campioni A De Luca EP Spugnini F Baldi R Cassandro, et al. 2006 Analysis of HtrA1 serine protease expression in human lung cancer Anticancer Res. 26 5A 3455 3459 17094466 1:CAS:528:DC%2BD28Xht1ersL3E
9. MA Bowden LA Di Nezza-Cossens T Jobling LA Salamonsen G Nie 2006 Serine proteases HTRA1 and HTRA3 are down-regulated with increasing grades of human endometrial cancer Gynecol Oncol. 103 1 253 260 16650464 10.1016/j.ygyno.2006. 03.006 1:CAS:528:DC%2BD28Xps1Wms74%3D
10. J Narkiewicz S Lapinska-Szumczyk D Zurawa-Janicka J Skorko-Glonek J Emerich B Lipinska 2009 Expression of human HtrA1, HtrA2, HtrA3 and TGF-beta1 genes in primary endometrial cancer Oncol Rep. 21 6 1529 1537 19424634 1:CAS:528:DC%2BD1MXmsVaqt70%3D
11. F Zhu L Jin TP Luo GH Luo Y Tan XH Qin 2010 Serine protease HtrA1 expression in human hepatocellular carcinoma Hepatobiliary Pancreat Dis Int. 9 5 508 512 20943460
12. YQ Liu XY Hu T Lu YN Cheng CY Young HQ Yuan, et al. 2012 Retigeric acid B exhibits antitumor activity through suppression of nuclear factor-kappaB signaling in prostate cancer cells in vitro and in vivo PLoS One. 7 5 e38000 22666431 10.1371/journal.pone.0038000 1:CAS:528:DC%2BC38Xot12rsrw%3D
13. A De Luca M De Falco V Fedele L Cobellis A Mastrogiacomo V Laforgia, et al. 2004 The serine protease HtrA1 is upregulated in the human placenta during pregnancy J Histochem Cytochem. 52 7 885 892 15208355 10.1369/jhc.3A6186.2004
14. Y Liu K Li Z Ren S Li H Zhang Q Fan 2012 Clinical implication of elevated human cervical cancer oncogene-1 expression in esophageal squamous cell carcinoma J Histochem Cytochem. 60 7 512 520 22511601
15. Zhao H, Yang J, Fan T, Li S, Ren X: RhoE functions as a tumor suppressor in esophageal squamous cell carcinoma and modulates the PTEN/PI3K/Akt signaling pathway. Tumour Biol 2012.
16. K Kataoka T Ono H Murata M Morishita KI Yamamoto M Sakaguchi, et al. 2012 S100A7 promotes the migration and invasion of osteosarcoma cells via the receptor for advanced glycation end products Oncol Lett. 3 5 1149 1153 22783409 1:CAS:528:DC%2BC38Xntlyhu7k%3D
17. HR Jin SZ Jin XF Cai D Li X Wu JX Nan, et al. 2012 Cryptopleurine targets NF-kappaB pathway, leading to inhibition of gene products associated with cell survival, proliferation, invasion, and angiogenesis PLoS One. 7 6 e40355 22768286 10.1371/journal.pone.0040355 1:CAS:528:DC%2BC38XpvVajtbc%3D
18. KJ Livak TD Schmittgen 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 4 402 408 11846609 10.1006/meth.2001.1262 1:CAS:528:DC%2BD38XhtFelt7s%3D
19. Z Lu H Liu L Xue P Xu T Gong G Hou 2008 An activated Notch1 signaling pathway inhibits cell proliferation and induces apoptosis in human esophageal squamous cell carcinoma cell line EC9706 Int J Oncol. 32 3 643 651 18292942 1:CAS:528:DC%2BD1cXjs1Cmurk%3D
20. G Hou Q Zhang L Wang M Liu J Wang L Xue 2010 mTOR inhibitor rapamycin alone or combined with cisplatin inhibits growth of esophageal squamous cell carcinoma in nude mice Cancer Lett. 290 2 248 254 19853373 10.1016/j.canlet. 2009.09.015 1:CAS:528:DC%2BC3cXivFGgu7Y%3D
21. MR Kang JS Kang JW Yang BG Kim JA Kim YN Jo, et al. 2012 Gene expression profiling of KBH-A42, a novel histone deacetylase inhibitor, in human leukemia and bladder cancer cell lines Oncol Lett. 3 1 113 118 22740865 1:CAS:528:DC%2BC38Xht1Slu7c%3D
22. MF Rubio PN Fernandez CV Alvarado LC Panelo MR Grecco GP Colo, et al. 2012 Cyclin D1 is a NF-kappaB corepressor Biochim Biophys Acta. 1823 6 1119 1131 22306268 10.1016/j.bbamcr.2012.01.009 1:CAS:528:DC%2BC38XntlygurY%3D
23. LJ Wang X Zhou W Wang F Tang CL Qi X Yang, et al. 2011 Andrographolide inhibits oral squamous cell carcinogenesis through NF-kappaB inactivation J Dent Res. 90 10 1246 1252 21841043 10.1177/0022034511418341 1:CAS:528: DC%2BC3MXhtlWqsLzN
24. P Yang L Guo ZJ Duan CG Tepper L Xue X Chen, et al. 2012 Histone methyltransferase NSD2/MMSET mediates constitutive NF-kappaB signaling for cancer cell proliferation, survival, and tumor growth via a feed-forward loop Mol Cell Biol. 32 15 3121 3131 22645312 10.1128/MCB.00204-12 1:CAS:528:DC%2BC38XhtFWjsLnL
25. Li F, Wang Y, Wang X, Li J, Cui H, Niu M: Ganoderic acids suppress growth and angiogenesis by modulating the NF-kappaB signaling pathway in breast cancer cells. Int J Clin Pharmacol Ther 2012.
26. Y Lu LM Wahl 2005 Production of matrix metalloproteinase-9 by activated human monocytes involves a phosphatidylinositol-3 kinase/Akt/IKKalpha/NF-kappaB pathway J Leukoc Biol. 78 1 259 265 15800029 10.1189/jlb.0904498 1:CAS:528:DC%2BD2MXmtFKntr8%3D
27. W Wang JL Abbruzzese DB Evans PJ Chiao 1999 Overexpression of urokinase-type plasminogen activator in pancreatic adenocarcinoma is regulated by constitutively activated RelA Oncogene 18 32 4554 4563 10467400 10.1038/sj.onc.1202833 1:CAS:528:DyaK1MXlslCrtbc%3D
28. SL Pomeroy P Tamayo M Gaasenbeek LM Sturla M Angelo ME McLaughlin, et al. 2002 Prediction of central nervous system embryonal tumour outcome based on gene expression Nature 415 6870 436 442 11807556 10.1038/415436a 1:CAS:528:DC%2BD38XhtVCqtr0%3D
29. D Zurawa-Janicka J Skorko-Glonek B Lipinska 2010 HtrA proteins as targets in therapy of cancer and other diseases Expert Opin Ther Targets. 14 7 665 679 20469960 10.1517/14728222.2010.487867 1:CAS:528:DC%2BC3cXntlGisrw%3D
30. SA Mullany M Moslemi-Kebria R Rattan A Khurana A Clayton T Ota, et al. 2011 Expression and functional significance of HtrA1 loss in endometrial cancer Clin Cancer Res. 17 3 427 436 21098697 10.1158/1078-0432.CCR-09-3069 1:CAS:528:DC%2BC3MXhsVersL4%3D
31. JB Welsh LM Sapinoso AI Su SG Kern J Wang-Rodriguez CA Moskaluk, et al. 2001 Hampton GM: analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer Cancer Res. 61 16 5974 5978 11507037 1:CAS:528:DC%2BD3MXmt12ktr8%3D
32. J Holzbeierlein P Lal E LaTulippe A Smith J Satagopan L Zhang, et al. 2004 Gene expression analysis of human prostate carcinoma during hormonal therapy identifies androgen-responsive genes and mechanisms of therapy resistance Am J Pathol. 164 1 217 227 14695335 10.1016/S0002-9440(10)63112-4 1:CAS:528:DC%2BD2cXlsVCnsA%3D%3D
33. YP Yu D Landsittel L Jing J Nelson B Ren L Liu, et al. 2004 Gene expression alterations in prostate cancer predicting tumor aggression and preceding development of malignancy J Clin Oncol. 22 14 2790 2799 15254046 10.1200/JCO.2004.05.158 1:CAS:528:DC%2BD2cXpsVWkt70%3D
34. S Varambally J Yu B Laxman DR Rhodes R Mehra SA Tomlins, et al. 2005 Integrative genomic and proteomic analysis of prostate cancer reveals signatures of metastatic progression Cancer Cell. 8 5 393 406 16286247 10.1016/j.ccr.2005.10.001 1:CAS:528:DC%2BD2MXht12gsbvE
35. Y Kotliarov ME Steed N Christopher J Walling Q Su A Center, et al. 2006 High-resolution global genomic survey of 178 gliomas reveals novel regions of copy number alteration and allelic imbalances Cancer Res. 66 19 9428 9436 17018597 10.1158/0008-5472.CAN-06-1691 1:CAS:528:DC%2BD28XhtVamsrjK
36. SH Kuo CH Chou AL Cheng CW Wang YH Chen RJ Chen 2012 Expression of BCL10 in cervical cancer has a role in the regulation of cell growth through the activation of NF-kappaB-dependent cyclin D1 signaling Gynecol Oncol. 126 2 245 251 22564715 10.1016/j.ygyno.2012.04.047 1:CAS:528:DC%2BC38Xns12qsbk%3D
37. FI Dimitrakopoulos AG Antonacopoulou A Kottorou H Vlotinou ND Panagopoulos D Dougenis, et al. 2012 NSCLC and the alternative pathway of NF-kappaB: uncovering an unknown relation Virchows Arch. 460 5 515 523 22562129 10.1007/s00428-012-1230-2 1:CAS:528:DC%2BC38XntVOltbc%3D
38. QL Tang XB Xie J Wang Q Chen AJ Han CY Zou, et al. 2012 Glycogen synthase kinase-3beta, NF-kappaB signaling, and tumorigenesis of human osteosarcoma J Natl Cancer Inst. 104 10 749 763 22534782 10.1093/jnci/djs210 1:CAS:528:DC%2BC38XnsFGitbg%3D
39. IC Allen JE Wilson M Schneider JD Lich RA Roberts JC Arthur, et al. 2012 NLRP12 suppresses colon inflammation and tumorigenesis through the negative regulation of noncanonical NF-kappaB signaling Immunity 36 5 742 754 22503542 10.1016/j.immuni.2012.03.012 1:CAS:528:DC%2BC38XlsVWrurs%3D
40. K Hinohara S Kobayashi H Kanauchi S Shimizu K Nishioka E Tsuji, et al. 2012 ErbB receptor tyrosine kinase/NF-kappaB signaling controls mammosphere formation in human breast cancer Proc Natl Acad Sci U S A. 109 17 6584 6589 22492965 10.1073/pnas.1113271109 1:CAS:528:DC%2BC38Xmslyjtbk%3D
41. FH Sarkar Y Li Z Wang D Kong 2008 NF-kappaB signaling pathway and its therapeutic implications in human diseases Int Rev Immunol. 27 5 293 319 18853341 10.1080/08830180802276179 1:CAS:528:DC%2BD1cXht1eksbfF
42. C Carbone D Melisi 2012 NF-kappaB as a target for pancreatic cancer therapy Expert Opin Ther Targets. 16 Suppl 2 S1 10 22443181 10.1517/14728222. 2011.645806 1:CAS:528:DC%2BC38XksFWmtLo%3D
43. YC Liu IT Chiang FT Hsu JJ Hwang 2012 Using NF-kappaB as a molecular target for theranostics in radiation oncology research Expert Rev Mol Diagn. 12 2 139 146 22369374 10.1586/erm.12.2 1:CAS:528:DC%2BC38XivFOru7o%3D
44. L Nogueira P Ruiz-Ontanon A Vazquez-Barquero F Moris JL Fernandez-Luna 2011 The NFkappaB pathway: a therapeutic target in glioblastoma Oncotarget 2 8 646 653 21896960
45. C Morais G Gobe DW Johnson H Healy 2011 The emerging role of nuclear factor kappa B in renal cell carcinoma Int J Biochem Cell Biol. 43 11 1537 1549 21854869 10.1016/j.biocel.2011.08.003 1:CAS:528:DC%2BC3MXht1Giu77N
46. W Chen Z Li L Bai Y Lin 2011 NF-kappaB in lung cancer, a carcinogenesis mediator and a prevention and therapy target Front Biosci. 16 1172 1185 21196225 10.2741/3782 1:CAS:528:DC%2BC3MXisVGnu7Y%3D
47. G Schneider OH Kramer 2011 NFkappaB/p53 crosstalk-a promising new therapeutic target Biochim Biophys Acta. 1815 1 90 103 20951769 1:CAS:528:DC%2BC3MXhtF2lsQ%3D%3D
48. M Breccia G Alimena 2010 NF-kappaB as a potential therapeutic target in myelodysplastic syndromes and acute myeloid leukemia Expert Opin Ther Targets. 14 11 1157 1176 20858024 10.1517/14728222.2010.522570 1:CAS:528: DC%2BC3cXht12ns7zE
49. X Wang K Belguise N Kersual KH Kirsch ND Mineva F Galtier, et al. 2007 Oestrogen signalling inhibits invasive phenotype by repressing RelB and its target BCL2 Nat Cell Biol. 9 4 470 478 17369819 10.1038/ncb1559 1:CAS:528:DC%2BD2sXjs12jsr8%3D
50. D Kong Z Wang SH Sarkar Y Li S Banerjee A Saliganan, et al. 2008 Platelet-derived growth factor-D overexpression contributes to epithelial-mesenchymal transition of PC3 prostate cancer cells Stem Cells. 26 6 1425 1435 18403754 10.1634/stemcells.2007-1076 1:CAS:528:DC%2BD1cXotFGhtL0%3D
51. P Poma M Notarbartolo M Labbozzetta R Sanguedolce A Alaimo V Carina, et al. 2006 Antitumor effects of the novel NF-kappaB inhibitor dehydroxymethyl- epoxyquinomicin on human hepatic cancer cells: analysis of synergy with cisplatin and of possible correlation with inhibition of pro-survival genes and IL-6 production Int J Oncol. 28 4 923 930 16525642 1:CAS:528: DC%2BD28XjtlCqtLg%3D
52. QG Dong GM Sclabas S Fujioka C Schmidt B Peng T Wu, et al. 2002 The function of multiple IkappaB:NF-kappaB complexes in the resistance of cancer cells to Taxol-induced apoptosis Oncogene 21 42 6510 6519 12226754 10.1038/sj.onc.1205848 1:CAS:528:DC%2BD38XmvVOqsbk%3D
53. G Helbig KW Christopherson 2nd 2003 Bhat-Nakshatri P, Kumar S, Kishimoto H, Miller KD, Broxmeyer HE, Nakshatri H: NF-kappaB promotes breast cancer cell migration and metastasis by inducing the expression of the chemokine receptor CXCR4 J Biol Chem. 278 24 21631 21638 12690099 10.1074/jbc.M300609200 1:CAS:528:DC%2BD3sXksVemsL8%3D
54. S Huang CA Pettaway H Uehara CD Bucana IJ Fidler 2001 Blockade of NF-kappaB activity in human prostate cancer cells is associated with suppression of angiogenesis, invasion, and metastasis Oncogene 20 31 4188 4197 11464285 10.1038/sj.onc.1204535 1:CAS:528:DC%2BD3MXls1WltbY%3D
55. RS Samant DW Clark RA Fillmore M Cicek BJ Metge KH Chandramouli, et al. 2007 Breast cancer metastasis suppressor 1 (BRMS1) inhibits osteopontin transcription by abrogating NF-kappaB activation Mol Cancer. 6 6 17227585 10.1186/1476-4598-6-6