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The hepatitis B virus X protein promotes tumor cell invasion by inducing membrane-type matrix metalloproteinase-1 and cyclooxygenase-2 expression

Enrique Lara-Pezzi, … , Alicia G. Arroyo, Manuel López-Cabrera

Enrique Lara-Pezzi, … , Alicia G. Arroyo, Manuel López-Cabrera

Published December 15, 2002
Citation Information: J Clin Invest. 2002;110(12):1831-1838. https://doi.org/10.1172/JCI15887.

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Article Infectious disease

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Citations to this article (81)

Title and authors	Publication	Year
Post-transplant HBV reactivation impacts the prognosis of patients with hepatitis B-related hepatocellular carcinoma: a dual-center retrospective cohort study in China. Li H, Lu D, Chen J, Zhang J, Zhuo J, Lin Z, Cao C, Shen W, He C, Chen H, Hu Z, Sun Y, Wei X, Zhuang L, Zheng S, Xu X	International journal of surgery (London, England)	2024
Exploring the mechanism of JiGuCao capsule formula on treating hepatitis B virus infection via network pharmacology analysis and in vivo/vitro experiment verification Cao X, Zhang N, Chen H, Wang W, Liang Y, Zhang J, Liu R, Li S, Yao Y, Jin Q, Guo Z, Chen Y, Gong Y, Li X, Zao X, Ye Y	Frontiers in pharmacology	2023
Hepatitis B Viral Protein HBx and the Molecular Mechanisms Modulating the Hallmarks of Hepatocellular Carcinoma: A Comprehensive Review. Sivasudhan E, Blake N, Lu Z, Meng J, Rong R	Cells	2022
The Role of Matrix Metalloproteinase in Inflammation with a Focus on Infectious Diseases. Lee HS, Kim WJ	International journal of molecular sciences	2022
Intracellular antibody targeting HBx suppresses invasion and metastasis in hepatitis B virus-related hepatocarcinogenesis via protein phosphatase 2A-B56γ-mediated dephosphorylation of protein kinase B. Che L, Du ZB, Wang WH, Wu JS, Han T, Chen YY, Han PY, Lei Z, Chen XX, He Y, Xu L, Lin X, Lin ZN, Lin YC	Cell Proliferation	2022
Multi-Faceted Roles of DNAJB Protein in Cancer Metastasis and Clinical Implications Kim HY, Hong S	International journal of molecular sciences	2022
Circ_DLEU2 knockdown represses cell proliferation, migration and invasion, and induces cell apoptosis through the miR-582-5p/COX2 pathway in acute myeloid leukemia. Dong S, Zhong H, Li L	Histology and histopathology	2022
HBV/HIV Coinfection: Impact on the Development and Clinical Treatment of Liver Diseases Z Cheng, P Lin, N Cheng	Frontiers in Medicine	2021
Cell death pathways and viruses: Role of microRNAs JS Nahand, L Shojaie, SA Akhlagh, MS Ebrahimi, HR Mirzaei, HB Baghi, M Mahjoubin-Tehran, N Rezaei, MR Hamblin, V Tajiknia, N Rahimian, H Mirzaei	Molecular Therapy — Nucleic Acids	2021
Relevance of reactive oxygen species in liver disease observed in transgenic mice expressing the hepatitis B virus X protein DY Yu	Laboratory animal research	2020
Single nucleotide polymorphism of rs2596542 and the risk of hepatocellular carcinoma development: A meta-analysis. Kuang XJ, Mo DC, Qin Y, Ahir BK, Wang JJ, Peng Z, Deng ZL	Medicine	2019
Relationship between the rs2596542 polymorphism in the MICA gene promoter and HBV/HCV infection-induced hepatocellular carcinoma: a meta-analysis. Luo X, Wang Y, Shen A, Deng H, Ye M	BMC Medical Genetics	2019
14-3-3 ζ binds to hepatitis B virus protein X and maintains its protein stability in hepatocellular carcinoma cells Y Tang, Y Zhang, C Wang, Z Sun, L Li, J Dong, W Zhou	Cancer Medicine	2018
Hepatitis B virus X protein-mediated non-coding RNA aberrations in the development of human hepatocellular carcinoma B Zhang, S Han, B Feng, X Chu, L Chen, R Wang	Experimental & molecular medicine	2017
The regulation of proteins associated with the cytoskeleton by hepatitis B virus X protein during hepatocarcinogenesis (Review) F Kong, H You, R Tang, K Zheng	Oncology Letters	2017
Hepatitis B virus X protein promotes hepatocellular carcinoma invasion and metastasis via upregulating thioredoxin interacting protein Z He, Y Yu, Y Nong, L Du, C Liu, Y Cao, L Bai, H Tang	Oncology Letters	2017
Fabrication, optimization, and characterization of umbelliferone β-D-galactopyranoside-loaded PLGA nanoparticles in treatment of hepatocellular carcinoma: in vitro and in vivo studies V Kumar, P Bhatt, M Rahman, G Kaithwas, H Choudhry, F Al-Abbasi, F Anwar, A Verma	International Journal of Nanomedicine	2017
Interferon‑α inhibits cell migration and invasion and induces the expression of antiviral proteins in Huh‑7 cells transfected with hepatitis B virus X gene‑expressing lentivirus Q Yang, XP Li, YB Zhong, TX Xiang, LL Zhang	Experimental and therapeutic medicine	2017
Influenza A viruses suppress cyclooxygenase-2 expression by affecting its mRNA stability SE Dudek, K Nitzsche, S Ludwig, C Ehrhardt	Scientific Reports	2016
Hepatitis B virus X protein in liver tumor microenvironment S Fu, R Zhou, N Li, Y Huang, XG Fan	Tumor Biology	2016
Hepatic SATB1 induces paracrine activation of hepatic stellate cells and is upregulated by HBx J Gong, W Tu, J Han, J He, J Liu, P Han, Y Wang, M Li, M Liu, J Liao, D Tian	Scientific Reports	2016
Nuclear IKKα mediates microRNA-7/-103/107/21 inductions to downregulate maspin expression in response to HBx overexpression WS Chen, LC Liu, CJ Yen, YJ Chen, JY Chen, CY Ho, SH Liu, CC Chen, WC Huang	Oncotarget	2016
miRNA-7/21/107 contribute to HBx-induced hepatocellular carcinoma progression through suppression of maspin WS Chen, CJ Yen, YJ Chen, JY Chen, LY Wang, SJ Chiu, WL Shih, CY Ho, TT Wei, HL Pan, PH Chien, CC Chen, MC Hung, WC Huang	Oncotarget	2015
Membrane Type 1 Matrix Metalloproteinase Regulates Monocyte Migration and Collagen Destruction in Tuberculosis T Sathyamoorthy, LB Tezera, NF Walker, S Brilha, L Saraiva, FA Mauri, RJ Wilkinson, JS Friedland, PT Elkington	Journal of immunology (Baltimore, Md. : 1950)	2015
Inhibitory effect of Phyllanthus urinaria L. extract on the replication of lamivudine-resistant hepatitis B virus in vitro J Jung, NK Kim, S Park, HJ Shin, SG Hwang, K Kim	BMC complementary and alternative medicine	2015
Important Role of the IL-32 Inflammatory Network in the Host Response against Viral Infection Y Zhou, Y Zhu	Viruses	2015
The Chinese medicine Sini-San inhibits HBx-induced migration and invasiveness of human hepatocellular carcinoma cells HJ Lin, ST Kao, YM Siao, CC Yeh	BMC complementary and alternative medicine	2015
Hepatitis B virus X protein specially regulates the sialyl lewis a synthesis among glycosylation events for metastasis TW Chung, SJ Kim, HJ Choi, KH Song, UH Jin, DY Yu, JK Seong, JG Kim, KJ Kim, JH Ko, KT Ha, YC Lee, CH Kim	Molecular Cancer	2014
MICA SNPs and the NKG2D system in virus-induced HCC K Goto, N Kato	Journal of Gastroenterology	2014
Tumour suppressor HLJ1: A potential diagnostic, preventive and therapeutic target in non-small cell lung cancer MF Tsai	World journal of clinical oncology	2014
COX-2-PGE2-EP receptor inflammatory axis: a key player in KSHV associated malignancies AG Paul, B Chandran, N Sharma-Walia	Translational Research	2013
Soluble interleukin-6 receptor-mediated innate immune response to DNA and RNA viruses Q Wang, X Chen, J Feng, Y Cao, Y Song, H Wang, C Zhu, S Liu, Y Zhu	Journal of virology	2013
HPV16 Oncoproteins Promote Cervical Cancer Invasiveness by Upregulating Specific Matrix Metalloproteinases J Kaewprag, W Umnajvijit, J Ngamkham, M Ponglikitmongkol, NK Karamanos	PloS one	2013
Hedgehog signaling blockade delays hepatocarcinogenesis induced by hepatitis B virus X (HBx) protein A Arzumanyan, V Sambandam, MM Clayton, SS Choi, G Xie, AM Diehl, DY Yu, MA Feitelson	Cancer research	2012
Follistatin-Like 3 Mediates Paracrine Fibroblast Activation by Cardiomyocytes KD Panse, LE Felkin, MM López-Olañeta, J Gómez-Salinero, M Villalba, L Muñoz, K Nakamura, M Shimano, K Walsh, PJ Barton, N Rosenthal, E Lara-Pezzi	Journal of Cardiovascular Translational Research	2012
Interaction of the hepatitis B spliced protein with cathepsin B promotes hepatoma cell migration and invasion WN Chen, JY Chen, BY Jiao, WS Lin, YL Wu, LL Liu, X Lin	Journal of virology	2012
Soluble MICA and a MICA variation as possible prognostic biomarkers for HBV-induced hepatocellular carcinoma V Kumar, PH Lo, H Sawai, N Kato, A Takahashi, Z Deng, Y Urabe, H Mbarek, K Tokunaga, Y Tanaka, M Sugiyama, M Mizokami, R Muroyama, R Tateishi, M Omata, K Koike, C Tanikawa, N Kamatani, M Kubo, Y Nakamura, K Matsuda	PloS one	2012
Role of hepatitis B virus X protein in regulating LIM and SH3 protein 1 (LASP-1) expression to mediate proliferation and migration of hepatoma cells R Tang, F Kong, L Hu, H You, P Zhang, W Du, K Zheng	Virology Journal	2012
Hepatitis B Virus X Protein Drives Multiple Cross-Talk Cascade Loops Involving NF-κB, 5-LOX, OPN and Capn4 to Promote Cell Migration X Zhang, X You, Q Wang, T Zhang, Y Du, N Lv, Z Zhang, S Zhang, C Shan, L Ye, X Zhang, WS Ryu	PloS one	2012
Diverse microbial interactions with the basement membrane barrier L Steukers, S Glorieux, AP Vandekerckhove, HW Favoreel, HJ Nauwynck	Trends in Microbiology	2012
Hepatitis B virus X protein promotes hepatoma cell invasion and metastasis by stabilizing Snail protein. Liu H, Xu L, He H, Zhu Y, Liu J, Wang S, Chen L, Wu Q, Xu J, Gu J	Cancer Science	2012
Induction of cyclooxygenase-2 expression by hepatitis B virus depends on demethylation-associated recruitment of transcription factors to the promoter X Yue, F Yang, Y Yang, Y Mu, W Sun, W Li, D Xu, J Wu, Y Zhu	Virology Journal	2011
Cyclooxygenase-2 −765 G/C polymorphisms and susceptibility to hepatitis B-related liver cancer in Han Chinese population J He, Q Zhang, Z Ren, Y Li, X Li, W Zhou, H Zhang, W Meng, J Yan, W He	Molecular Biology Reports	2011
Tumor initiation and progression in hepatocellular carcinoma: risk factors, classification, and therapeutic targets T Severi, H Malenstein, C Verslype, JF van Pelt	Acta Pharmacologica Sinica	2010
Hepatitis B virus X protein upregulates HSP90alpha expression via activation of c-Myc in human hepatocarcinoma cell line, HepG2 W Li, X Miao, Z Qi, W Zeng, J Liang, Z Liang	Virology Journal	2010
Hypoxia, angiogenesis and liver fibrogenesis in the progression of chronic liver diseases C Paternostro, E David, E Novo, M Parola	World journal of gastroenterology : WJG	2010
A mutant of hepatitis B virus X protein (HBxΔ127) enhances hepatoma cell migration via osteopontin involving 5-lipoxygenase X Zhang, L Ye, X Zhang	Acta Pharmacologica Sinica	2010
The Tumor Microenvironment in Hepatocellular Carcinoma: Current Status and Therapeutic Targets JD Yang, I Nakamura, LR Roberts	Seminars in Cancer Biology	2010
Overexpression of cyclooxygenase-2 in noncancerous liver tissue increases the postoperative recurrence of hepatocellular carcinoma in patients with hepatitis B virus-related cirrhosis. He YF, Jin J, Wei W, Chang Y, Hu B, Ji CS, Jia WD, Wang XQ, Chen K, Chen J	Canadian journal of gastroenterology = Journal canadien de gastroenterologie	2010
Pulmonary surfactant: an immunological perspective ZC Chroneos, Z Sever-Chroneos, VL Shepherd	Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology	2009
Putative roles of hepatitis B x antigen in the pathogenesis of chronic liver disease MA Feitelson, HM Reis, NL Tufan, B Sun, J Pan, Z Lian	Cancer Letters	2009
Gene expression profiles of human liver cells mediated by hepatitis B virus X protein W Zhang, F Xu, C Shan, R Xiang, L Ye, X Zhang	Acta Pharmacologica Sinica	2009
Transformation of human liver L-O2 cells mediated by stable HBx transfection W Zhang, N Cai, L Ye, X Zhang	Acta Pharmacologica Sinica	2009
HBx targeting to mitochondria and ROS generation are necessary but insufficient for HBV-induced cyclooxygenase-2 expression W Lim, SH Kwon, H Cho, S Kim, S Lee, WS Ryu, H Cho	Journal of Molecular Medicine	2009
Cyclooxygenase-2 Mediates Dialysate-Induced Alterations of the Peritoneal Membrane LS Aroeira, E Lara-Pezzi, J Loureiro, A Aguilera, M Ramírez-Huesca, G González-Mateo, ML Pérez-Lozano, P Albar-Vizcaíno, MA Bajo, G del Peso, JA Sánchez-Tomero, JA Jiménez-Heffernan, R Selgas, M López-Cabrera	Journal of the American Society of Nephrology : JASN	2009
Transforming growth factor-beta gene expression signature in mouse hepatocytes predicts clinical outcome in human cancer C Coulouarn, VM Factor, SS Thorgeirsson	Hepatology	2008
NS3 protein of hepatitis C virus regulates cyclooxygenase-2 expression through multiple signaling pathways L Lu, L Wei, G Peng, Y Mu, K Wu, L Kang, X Yan, Y Zhu, J Wu	Virology	2008
Differential effects of triptolide and tetrandrine on activation of COX-2, NF-κB, and AP-1 and virus production in dengue virus-infected human lung cells JT Liou, ZY Chen, LJ Ho, SP Yang, DM Chang, CC Liang, JH Lai	European Journal of Pharmacology	2008
Identification of Softness Syndrome-Associated Candidate Genes and DNA Sequence Variation in the Sea Squirt, Halocynthia roretzi HK Cho, BH Nam, HJ Kong, HS Han, YB Hur, TJ Choi, YH Choi, WJ Kim, JH Cheong	Marine Biotechnology	2008
Activation of Interleukin-32 Pro-Inflammatory Pathway in Response to Influenza A Virus Infection W Li, Y Liu, MM Mukhtar, R Gong, Y Pan, ST Rasool, Y Gao, L Kang, Q Hao, G Peng, Y Chen, X Chen, J Wu, Y Zhu, RC May	PloS one	2008
A naturally occurring calcineurin variant inhibits FoxO activity and enhances skeletal muscle regeneration E Lara-Pezzi, N Winn, A Paul, K McCullagh, E Slominsky, MP Santini, F Mourkioti, P Sarathchandra, S Fukushima, K Suzuki, N Rosenthal	The Journal of Cell Biology	2007
Molecular Pathogenesis of Hepatitis-B-virus-associated Hepatocellular Carcinoma NH Park, IH Song, YH Chung	Gut and Liver	2007
Hepatitis B virus promotes angiopoietin-2 expression in liver tissue: role of HBV x protein P Sanz-Cameno, S Martín-Vílchez, E Lara-Pezzi, MJ Borque, J Salmerón, PM de Rueda, JA Solís, M López-Cabrera, R Moreno-Otero	The American Journal of Pathology	2006
Activation of focal adhesion kinase by hepatitis B virus HBx protein: multiple functions in viral replication MJ Bouchard, L Wang, RJ Schneider	Journal of virology	2006
Chronic hepatitis B in hepatocarcinogenesis NH Park, IH Song, YH Chung	Postgraduate medical journal	2006
Cyclooxygenase 2 induced by Kaposi's sarcoma-associated herpesvirus early during in vitro infection of target cells plays a role in the maintenance of latent viral gene expression N Sharma-Walia, H Raghu, S Sadagopan, R Sivakumar, MV Veettil, PP Naranatt, MM Smith, B Chandran	Journal of virology	2006
Nucleocapsid protein of SARS-CoV activates the expression of cyclooxygenase-2 by binding directly to regulatory elements for nuclear factor-kappa B and CCAAT/enhancer binding protein X Yan, Q Hao, Y Mu, KA Timani, L Ye, Y Zhu, J Wu	The International Journal of Biochemistry & Cell Biology	2006
Gene Expression Analysis in HBV Transgenic Mouse Liver: A Model to Study Early Events Related to Hepatocarcinogenesis M Barone, D Spano, M DApolito, M Centra, C Lasalandra, M Capasso, AD Leo, S Volinia, D Arcelli, N Rosso, A Franavilla, C Tiribelli, A Iolascon	Molecular Medicine	2006
Cyclooxygenases in hepatocellular carcinoma. Cervello M, Montalto G	World Journal of Gastroenterology	2006
Amino acids 1 to 422 of the spike protein of SARS associated coronavirus are required for induction of cyclooxygenase-2. Liu M, Gu C, Wu J, Zhu Y	Virus Genes	2006
Chemoprevention of spontaneous development of hepatocellular carcinomas in fatty liver Shionogi mice by a cyclooxygenase‐2 inhibitor Liu W, Nakamura H, Tsujimura T, Cheng J, Yamamoto T, Iwamoto Y, Imanishi H, Shimomura S, Yamamoto T, Hirasawa T, Inagaki S, Nishiguchi S, Hada T	Cancer Science	2006
Hepatitis C Virus Stimulates the Expression of Cyclooxygenase-2 via Oxidative Stress: Role of Prostaglandin E 2 in RNA Replication G Waris, A Siddiqui	Journal of virology	2005
The paradox of matrix metalloproteinases in infectious disease PT Elkington, CM O'Kane, JS Friedland	Clinical & Experimental Immunology	2005
Tumor cyclooxygenase-2 levels correlate with tumor invasiveness in human hepatocellular carcinoma. Tang TC, Poon RT, Lau CP, Xie D, Fan ST	World Journal of Gastroenterology	2005
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Mechanism of metastasis by membrane type 1-matrix metalloproteinase in hepatocellular carcinoma. Ip YC, Cheung ST, Leung KL, Fan ST	World Journal of Gastroenterology	2005
Increased intrahepatic cyclooxygenase 2, matrix metalloproteinase 2, and matrix metalloproteinase 9 expression is associated with progressive liver disease in chronic hepatitis C virus infection: role of viral core and NS5A proteins O Núñez, A Fernández-Martínez, PL Majano, A Apolinario, M Gómez-Gonzalo, I Benedicto, M López-Cabrera, L Boscá, G Clemente, C García-Monzón, P Martín-Sanz	Gut	2004
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Activating mechanism of transcriptor NF-kappaB regulated by hepatitis B virus X protein in hepatocellular carcinoma. Wang T, Wang Y, Wu MC, Guan XY, Yin ZF	World Journal of Gastroenterology	2004
Recent progress in predictive biomarkers for metastatic recurrence of human hepatocellular carcinoma: a review of the literature. Qin LX, Tang ZY	Journal of Cancer Research and Clinical Oncology	2004
COX-2 induction during murine gammaherpesvirus 68 infection leads to enhancement of viral gene expression TL Symensma, DA Martinez-Guzman, Q Jia, E Bortz, TT Wu, N Rudra-Ganguly, S Cole, H Herschman, R Sun	Journal of virology	2003

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