Lentiviral vector mediated claudin1 silencing inhibits epithelial to mesenchymal transition in breast cancer cells

Viruses

Volumn 7, Issue 6, 2015, Pages 2965-2979

  Zhao, Xianqi ^a,b   Zou, Yanan ^a,b   Gu, Qingqing ^b   Zhao, Guannan ^b   Gray, Horace ^b   Pfeffer, Lawrence M ^b   Yue, Junming ^b  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Breast cancer; CLDN1; Epithelial to mesenchymal transition

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CLAUDIN 1; LENTIVIRUS VECTOR; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR SLUG; UVOMORULIN; ANTINEOPLASTIC AGENT; CLDN1 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ARTICLE; BREAST CANCER; CANCER GENE THERAPY; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE SILENCING; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; RNA INTERFERENCE; TUMOR GROWTH; UPREGULATION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; BREAST NEOPLASMS; CELL MOTION; DRUG EFFECTS; EPITHELIUM CELL; FEMALE; GENE VECTOR; GENETIC TRANSFORMATION; GENETICS; LENTIVIRINAE; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CLAUDIN-1; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE SILENCING; GENETIC VECTORS; HUMANS; LENTIVIRUS; MODELS, BIOLOGICAL; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSFORMATION, GENETIC;

EID: 84931292236     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7062755     Document Type: Article

References (43)

1. Chatenoud, L.; Bertuccio, P.; Bosetti, C.; Malvezzi, M.; Levi, F.; Negri, E.; la Vecchia, C. Trends in mortality from major cancers in the Americas: 1980-2010. Ann. Oncol. 2014, 25, 1843-1853. [CrossRef] [PubMed]
2. Lares, M.R.; Rossi, J.J.; Ouellet, D.L. RNAi and small interfering RNAs in human disease therapeutic applications. Trends Biotechnol. 2010, 28, 570-579. [CrossRef] [PubMed]
3. Xie, Y.; Hicks, M.J.; Kaminsky, S.M.; Moore, M.A.; Crystal, R.G.; Rafii, A. AAV-mediated persistent bevacizumab therapy suppresses tumor growth of ovarian cancer. Gynecol. Oncol. 2014, 135, 325-332. [CrossRef] [PubMed]
4. Majhen, D.; Calderon, H.; Chandra, N.; Fajardo, C.A.; Rajan, A.; Alemany, R.; Custers, J. Adenovirus-based vaccines for fighting infectious diseases and cancer: Progress in the field. Hum. Gene Ther. 2014, 25, 301-317. [CrossRef] [PubMed]
5. Kaufmann, J.K.; Chiocca, E.A. Glioma virus therapies between bench and bedside. Neuro Oncol. 2014, 16, 334-351. [CrossRef] [PubMed]
6. Zolotukhin, I.; Luo, D.; Gorbatyuk, O.; Hoffman, B.; Warrington, K., Jr.; Herzog, R.; Harrison, J.; Cao, O. Improved Adeno-associated Viral Gene Transfer to Murine Glioma. J. Genet. Syndr. Gene Ther. 2013, 4, e12815.
7. Piccioni, D.E.; Kesari, S. Clinical trials of viral therapy for malignant gliomas. Expert Rev. Anticancer Ther. 2013, 13, 1297-1305. [CrossRef] [PubMed]
8. Kim, H.S.; Kim, C.H.; Park, M.Y.; Park, J.S.; Park, H.M.; Sohn, H.J.; Kim, H.J.; Kim, S.G.; Oh, S.T.; Kim, T.G. Efficient co-transduction of adenoviral vectors encoding carcinoembryonic antigen and survivin into dendritic cells by the CAR-TAT adaptor molecule enhance anti-tumor immunity in a murine colorectal cancer model. Immunol. Lett. 2010, 131, 73-80. [CrossRef] [PubMed]
9. Yue, J.; Sheng, Y.; Ren, A.; Penmatsa, S. A miR-21 hairpin structure-based gene knockdown vector. Biochem. Biophys. Res. Commun. 2010, 394, 667-672. [CrossRef] [PubMed]
10. Stegmeier, F.; Hu, G.; Rickles, R.J.; Hannon, G.J.; Elledge, S.J. A lentiviral microRNA-based system for single-copy polymerase II-regulated RNA interference in mammalian cells. Proc. Natl. Acad. Sci. USA 2005, 102, 13212-13217. [CrossRef] [PubMed]
11. Liechtenstein, T.; Perez-Janices, N.; Escors, D. Lentiviral vectors for cancer immunotherapy and clinical applications. Cancers 2013, 5, 815-837. [CrossRef] [PubMed]
12. Szabo, I.; Kiss, A.; Schaff, Z.; Sobel, G. Claudins as diagnostic and prognostic markers in gynecological cancer. Histol. Histopathol. 2009, 24, 1607-1615. [PubMed]
13. Pope, J.L.; Ahmad, R.; Bhat, A.A.; Washington, M.K.; Singh, A.B.; Dhawan, P. Claudin-1 overexpression in intestinal epithelial cells enhances susceptibility to adenamatous polyposis coli-mediated colon tumorigenesis. Mol. Cancer 2014, 13, e167. [CrossRef] [PubMed]
14. Jing, P.; Zou, J.; Zhang, J.; Jiang, X. DeltaNp63 promotes UMUC3 cell invasiveness and migration through claudin1 in vitro. Mol. Med. Rep. 2013, 7, 1026-1030. [PubMed]
15. Iitaka, D.; Moodley, S.; Shimizu, H.; Bai, X.H.; Liu, M. PKCdelta-iPLA2-PGE2-PPARgamma signaling cascade mediates TNF-alpha induced Claudin 1 expression in human lung carcinoma cells. Cell Signal. 2015, 27, 568-577. [CrossRef] [PubMed]
16. Huang, J.; Zhang, L.; He, C.; Qu, Y.; Li, J.; Zhang, J.; Du, T.; Chen, X.; Yu, Y.; Liu, B.; et al. Claudin-1 enhances tumor proliferation and metastasis by regulating cell anoikis in gastric cancer. Oncotarget 2014, 6, 1652-1665.
17. Qin, W.; Ren, Q.; Liu, T.; Huang, Y.; Wang, J. MicroRNA-155 is a novel suppressor of ovarian cancer-initiating cells that targets CLDN1. FEBS Lett. 2013, 587, 1434-1439. [CrossRef] [PubMed]
18. Leotlela, P.D.; Wade, M.S.; Duray, P.H.; Rhode, M.J.; Brown, H.F.; Rosenthal, D.T.; Dissanayake, S.K.; Earley, R.; Indig, F.E.; Nickoloff, B.J.; et al. Claudin-1 overexpression in melanoma is regulated by PKC and contributes to melanoma cell motility. Oncogene 2007, 26, 3846-3856. [CrossRef] [PubMed]
19. Nakagawa, S.; Miyoshi, N.; Ishii, H.; Mimori, K.; Tanaka, F.; Sekimoto, M.; Doki, Y.; Mori, M. Expression of CLDN1 in colorectal cancer: A novel marker for prognosis. Int. J. Oncol. 2011, 39, 791-796. [PubMed]
20. Blanchard, A.A.; Watson, P.H.; Shiu, R.P.; Leygue, E.; Nistor, A.; Wong, P.; Myal, Y. Differential expression of claudin 1, 3, and 4 during normal mammary gland development in the mouse. DNA Cell Biol. 2006, 25, 79-86. [CrossRef] [PubMed]
21. Morohashi, S.; Kusumi, T.; Sato, F.; Odagiri, H.; Chiba, H.; Yoshihara, S.; Hakamada, K.; Sasaki, M.; Kijima, H. Decreased expression of claudin-1 correlates with recurrence status in breast cancer. Int. J. Mol. Med. 2007, 20, 139-143. [CrossRef] [PubMed]
22. Ma, F.; Ding, X.; Fan, Y.; Ying, J.; Zheng, S.; Lu, N.; Xu, B. A CLDN1-negative phenotype predicts poor prognosis in triple-negative breast cancer. PLoS ONE 2014, 9, e112765. [CrossRef] [PubMed]
23. Blanchard, A.A.; Ma, X.; Dueck, K.J.; Penner, C.; Cooper, S.C.; Mulhall, D.; Murphy, L.C.; Leygue, E.; Myal, Y. Claudin 1 expression in basal-like breast cancer is related to patient age. BMC Cancer 2013, 13, e268. [CrossRef] [PubMed]
24. Akasaka, H.; Sato, F.; Morohashi, S.; Wu, Y.; Liu, Y.; Kondo, J.; Odagiri, H.; Hakamada, K.; Kijima, H. Anti-apoptotic effect of claudin-1 in tamoxifen-treated human breast cancer MCF-7 cells. BMC Cancer 2010, 10, e548. [CrossRef] [PubMed]
25. Canadas, I.; Rojo, F.; Taus, A.; Arpi, O.; Arumi-Uria, M.; Pijuan, L.; Menendez, S.; Zazo, S.; Domine, M.; Salido, M.; et al. Targeting epithelial-to-mesenchymal transition with Met inhibitors reverts chemoresistance in small cell lung cancer. Clin. Cancer Res. 2014, 20, 938-950. [CrossRef] [PubMed]
26. Kajiyama, H.; Shibata, K.; Terauchi, M.; Yamashita, M.; Ino, K.; Nawa, A.; Kikkawa, F. Chemoresistance to paclitaxel induces epithelial-mesenchymal transition and enhances metastatic potential for epithelial ovarian carcinoma cells. Int. J. Oncol. 2007, 31, 277-283. [CrossRef] [PubMed]
27. Gungor, C.; Zander, H.; Effenberger, K.E.; Vashist, Y.K.; Kalinina, T.; Izbicki, J.R.; Yekebas, E.; Bockhorn, M. Notch signaling activated by replication stress-induced expression of midkine drives epithelial-mesenchymal transition and chemoresistance in pancreatic cancer. Cancer Res. 2011, 71, 5009-5019. [CrossRef] [PubMed]
28. Glackin, C.A. Targeting the Twist and Wnt signaling pathways in metastatic breast cancer. Maturitas 2014, 79, 48-51. [CrossRef] [PubMed]
29. Korsching, E.; Packeisen, J.; Liedtke, C.; Hungermann, D.; Wulfing, P.; van Diest, P.J.; Brandt, B.; Boecker, W.; Buerger, H. The origin of vimentin expression in invasive breast cancer: Epithelial-mesenchymal transition, myoepithelial histogenesis or histogenesis from progenitor cells with bilinear differentiation potential? J. Pathol. 2005, 206, 451-457. [CrossRef] [PubMed]
30. Tiwari, N.; Meyer-Schaller, N.; Arnold, P.; Antoniadis, H.; Pachkov, M.; van Nimwegen, E.; Christofori, G. Klf4 is a transcriptional regulator of genes critical for EMT, including Jnk1 (Mapk8). PLoS ONE 2013, 8, e57329. [CrossRef] [PubMed]
31. Pinho, A.V.; Rooman, I.; Real, F.X. p53-dependent regulation of growth, epithelial-mesenchymal transition and stemness in normal pancreatic epithelial cells. Cell Cycle 2011, 10, 1312-1321. [CrossRef] [PubMed]
32. Wellner, U.; Schubert, J.; Burk, U.C.; Schmalhofer, O.; Zhu, F.; Sonntag, A.; Waldvogel, B.; Vannier, C.; Darling, D.; zur Hausen, A.; et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell Biol. 2009, 11, 1487-1495. [CrossRef] [PubMed]
33. Guo, Y.; Tian, P.; Yang, C.; Liang, Z.; Li, M.; Sims, M.; Lu, L.; Zhang, Z.; Li, H.; Pfeffer, L.M.; et al. Silencing the Double-Stranded RNA Binding Protein DGCR8 Inhibits Ovarian Cancer Cell Proliferation, Migration, and Invasion. Pharm. Res. 2015, 32, 769-778. [CrossRef] [PubMed]
34. Chen, Z.; Wang, Y.; Liu, W.; Zhao, G.; Lee, S.; Balogh, A.; Zou, Y.; Guo, Y.; Zhang, Z.; Gu, W.; et al. Doxycycline inducible Kruppel-like factor 4 lentiviral vector mediates mesenchymal to epithelial transition in ovarian cancer cells. PLoS ONE 2014, 9, e105331. [CrossRef] [PubMed]
35. Myal, Y.; Leygue, E.; Blanchard, A.A. Claudin 1 in breast tumorigenesis: Revelation of a possible novel "claudin high" subset of breast cancers. J. Biomed. Biotechnol. 2010, 2010, e956897. [CrossRef] [PubMed]
36. Heerma van Voss, M.R.; van Diest, P.J.; Smolders, Y.H.; Bart, J.; van derWall, E.; van der Groep, P. Distinct claudin expression characterizes BRCA1-related breast cancer. Histopathology 2014, 65, 814-827. [CrossRef] [PubMed]
37. Lu, S.; Singh, K.; Mangray, S.; Tavares, R.; Noble, L.; Resnick, M.B.; Yakirevich, E. Claudin expression in high-grade invasive ductal carcinoma of the breast: Correlation with the molecular subtype. Mod. Pathol. 2013, 26, 485-495. [CrossRef] [PubMed]
38. Blanchard, A.A.; Skliris, G.P.; Watson, P.H.; Murphy, L.C.; Penner, C.; Tomes, L.; Young, T.L.; Leygue, E.; Myal, Y. Claudins 1, 3, and 4 protein expression in ER negative breast cancer correlates with markers of the basal phenotype. Virchows Arch. 2009, 454, 647-656. [CrossRef] [PubMed]
39. Di Cello, F.; Cope, L.; Li, H.; Jeschke, J.;Wang,W.; Baylin, S.B.; Zahnow, C.A. Methylation of the claudin 1 promoter is associated with loss of expression in estrogen receptor positive breast cancer. PLoS ONE 2013, 8, e68630. [CrossRef] [PubMed]
40. Liu, Y.; Wang, L.; Lin, X.Y.; Wang, J.; Yu, J.H.; Miao, Y.; Wang, E.H. Anti-apoptotic effect of claudin-1 on TNF-alpha-induced apoptosis in human breast cancer MCF-7 cells. Tumour Biol. 2012, 33, 2307-2315. [CrossRef] [PubMed]
41. Hoevel, T.; Macek, R.; Swisshelm, K.; Kubbies, M. Reexpression of the TJ protein CLDN1 induces apoptosis in breast tumor spheroids. Int. J. Cancer 2004, 108, 374-383. [CrossRef] [PubMed]
42. Martinez-Estrada, O.M.; Culleres, A.; Soriano, F.X.; Peinado, H.; Bolos, V.; Martinez, F.O.; Reina, M.; Cano, A.; Fabre, M.; Vilaro, S. The transcription factors Slug and Snail act as repressors of Claudin-1 expression in epithelial cells. Biochem. J. 2006, 394, 449-457. [PubMed]
43. Van Pham, P.; Vu, N.B.; Duong, T.T.; Nguyen, T.T.; Truong, N.H.; Phan, N.L.; Vuong, T.G.; Pham, V.Q.; Nguyen, H.M.; Nguyen, K.T.; et al. Suppression of human breast tumors in NOD/SCID mice by CD44 shRNA gene therapy combined with doxorubicin treatment. OncoTargets Ther. 2012, 5, 77-84. [CrossRef] [PubMed]