Folate-linked lipoplexes for short hairpin RNA targeting claudin-3 delivery in ovarian cancer xenografts

Journal of Controlled Release

Volumn 172, Issue 3, 2013, Pages 679-689

  He, Zhi Yao ^a   Wei, Xia Wei ^b   Luo, Min ^a   Luo, Shun Tao ^a   Yang, Yang ^b   Yu, Yi Yi ^b   Chen, Yan ^a   Ma, Cui Cui ^a   Liang, Xiao ^a   Guo, Fu Chun ^a   Ye, Ting Hong ^a   Shi, Hua Shan ^a   Shen, Guo Bo ^a   Wang, Wei ^a   Gong, Feng Ming ^a   He, Gu ^a   Yang, Li ^a   Zhao, Xia ^b   Song, Xiang Rong ^a   Wei, Yu Quan ^a  

^a SICHUAN UNIVERSITY   (China)

^b SICHUAN UNIVERSITY   (China)

Author keywords

Claudin3; Folate receptor ; Gene therapy; Lipoplex; Ovarian cancer

Indexed keywords

ANTITUMOR MECHANISMS; CLAUDIN3; FOLATE RECEPTOR; LIPOPLEXES; MICROVESSEL DENSITY; OVARIAN CANCERS; SAFETY EVALUATIONS; SHORT HAIRPIN RNA (SHRNA);

CELL DEATH; CELL PROLIFERATION; DISEASES; GENE THERAPY; LIPOSOMES; LOADING; RNA; TUMORS;

DIAGNOSIS;

CLAUDIN 3; FOLATE RECEPTOR 1; FOLIC ACID; LIPOPLEX; SHORT HAIRPIN RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER TISSUE; CAPILLARY DENSITY; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG FORMULATION; DRUG SAFETY; FEMALE; GENE EXPRESSION; GENE FUNCTION; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIPOSOMAL DELIVERY; MALIGNANT ASCITES; MOUSE; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; TUMOR CELL; TUMOR DIFFERENTIATION; TUMOR VOLUME; TUMOR XENOGRAFT;

CLAUDIN3; FOLATE RECEPTOR Α; GENE THERAPY; LIPOPLEX; OVARIAN CANCER;

ANIMALS; BREAST; CELL LINE, TUMOR; CLAUDIN-3; FEMALE; FOLIC ACID; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC THERAPY; HUMANS; MICE, INBRED BALB C; MICE, NUDE; OVARIAN NEOPLASMS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 84887194875     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.10.015     Document Type: Article

References (45)

1. E.M.J.J. Berns, and D.D. Bowtell The changing view of high-grade serous ovarian cancer Cancer Res. 72 2012 2701 2704
2. J. Kang, A.D. D'Andrea, and D. Kozono A DNA repair pathway-focused score for prediction of outcomes in ovarian cancer treated with platinum-based chemotherapy J. Natl. Cancer Inst. 104 2012 670 681
3. The Journal of Gene Medicine: gene therapy clinical trials worldwide Available at: http://www.abedia.com/wiley/index.html 2013 (Accessed September 21, 2013)
4. A.B. Singh, A. Sharma, and P. Dhawan Claudin family of proteins and cancer: an overview J. Oncol. 2010 2010 541957
5. S.L. Kominsky Claudins: emerging targets for cancer therapy Expert Rev. Mol. Med. 8 2006 1 11 (Pubitemid 44184255)
6. A. Ouban, and A. Ahmed Claudins in human cancer: a review Histol. Histopathol. 25 2010 83 90
7. Y.-H. Huang, Y. Bao, W. Peng, M. Goldberg, K. Love, D.A. Bumcrot, G. Cole, R. Langer, D.G. Anderson, and J.A. Sawicki Claudin-3 gene silencing with siRNA suppresses ovarian tumor growth and metastasis Proc. Natl. Acad. Sci. U. S. A. 106 2009 3426 3430
8. L. Kleinberg, A. Holth, C.G. Trope, R. Reich, and B. Davidson Claudin upregulation in ovarian carcinoma effusions is associated with poor survival Hum. Pathol. 39 2008 747 757 (Pubitemid 351618309)
9. P.J. Morin Claudin proteins in human cancer: promising new targets for diagnosis and therapy Cancer Res. 65 2005 9603 9606 (Pubitemid 41541431)
10. I.R. Gupta, and A.K. Ryan Claudins: unlocking the code to tight junction function during embryogenesis and in disease Clin. Genet. 77 2010 314 325
11. C. Sun, T. Yi, X. Song, S. Li, X. Qi, X. Chen, H. Lin, X. He, Z. Li, Y. Wei, and X. Zhao Efficient inhibition of ovarian cancer by short hairpin RNA targeting claudin-3 Oncol. Rep. 26 2011 193 200
12. J. Hrkach, D. Von Hoff, M.M. Ali, E. Andrianova, J. Auer, T. Campbell, D. De Witt, M. Figa, M. Figueiredo, A. Horhota, S. Low, K. McDonnell, E. Peeke, B. Retnarajan, A. Sabnis, E. Schnipper, J.J. Song, Y.H. Song, J. Summa, D. Tompsett, G. Troiano, T. Van Geen Hoven, J. Wright, P. LoRusso, P.W. Kantoff, N.H. Bander, C. Sweeney, O.C. Farokhzad, R. Langer, and S. Zale Preclinical development and clinical translation of a PSMA-targeted docetaxel nanoparticle with a differentiated pharmacological profile Sci. Transl. Med. 4 2012 128ra139
13. J.-H. Kim, S.M. Bae, M.-H. Na, H. Shin, Y.J. Yang, K.H. Min, K.Y. Choi, K. Kim, R.-W. Park, I.C. Kwon, B.-H. Lee, A.S. Hoffman, and I.-S. Kim Facilitated intracellular delivery of peptide-guided nanoparticles in tumor tissues J. Control. Release 157 2012 493 499
14. H. Lee, A.K.R. Lytton-Jean, Y. Chen, K.T. Love, A.I. Park, E.D. Karagiannis, A. Sehgal, W. Querbes, C.S. Zurenko, M. Jayaraman, C.G. Peng, K. Charisse, A. Borodovsky, M. Manoharan, J.S. Donahoe, J. Truelove, M. Nahrendorf, R. Langer, and D.G. Anderson Molecularly self-assembled nucleic acid nanoparticles for targeted in vivo siRNA delivery Nat. Nanotechnol. 7 2012 389 393
15. S. Lee, J. Kim, G. Shim, S. Kim, S.E. Han, K. Kim, I.C. Kwon, Y. Choi, Y.B. Kim, C.-W. Kim, and Y.-K. Oh Tetraiodothyroacetic acid-tagged liposomes for enhanced delivery of anticancer drug to tumor tissue via integrin receptor J. Control. Release 164 2012 213 220
16. Z. Cheng, A. Al Zaki, J.Z. Hui, V.R. Muzykantov, and A. Tsourkas Multifunctional nanoparticles: cost versus benefit of adding targeting and imaging capabilities Science 338 2012 903 910
17. P.S. Low, and S.A. Kularatne Folate-targeted therapeutic and imaging agents for cancer Curr. Opin. Chem. Biol. 13 2009 256 262
18. M.K.Y. Siu, D.S.H. Kong, H.Y. Chan, E.S.Y. Wong, P.P.C. Ip, L. Jiang, H.Y.S. Ngan, X.-F. Le, and A.N.Y. Cheung Paradoxical impact of two folate receptors, FRα and RFC, in ovarian cancer: effect on cell proliferation, invasion and clinical outcome PLoS ONE 7 2012 e47201
19. L. Teng, J. Xie, L. Teng, and R.J. Lee Clinical translation of folate receptor-targeted therapeutics Expert Opin. Drug Deliv. 9 2012 901 908
20. L. Kandalaft, D. Powell, and G. Coukos A phase I clinical trial of adoptive transfer of folate receptor-alpha redirected autologous T cells for recurrent ovarian cancer J. Transl. Med. 10 2012 157
21. H. Arima, A. Yoshimatsu, H. Ikeda, A. Ohyama, K. Motoyama, T. Higashi, A. Tsuchiya, T. Niidome, Y. Katayama, K. Hattori, and T. Takeuchi Folate-PEG-appended dendrimer conjugate with α-cyclodextrin as a novel cancer cell-selective siRNA delivery carrier Mol. Pharm. 9 2012 2591 2604
22. S. Zou, N. Cao, D. Cheng, R. Zheng, J. Wang, K. Zhu, and X. Shuai Enhanced apoptosis of ovarian cancer cells via nanocarrier-mediated codelivery of siRNA and doxorubicin Int. J. Nanomedicine 7 2012 3823 3835
23. J. Li, Z. He, S. Yu, S. Li, Q. Ma, Y. Yu, J. Zhang, R. Li, Y. Zheng, G. He, and X. Song Micelles based on methoxy poly(ethylene glycol) cholesterol conjugate for controlled and targeted drug delivery of a poorly water soluble drug J. Biomed. Nanotechnol. 8 2012 809 817
24. Z. He, Y. Yu, Y. Zhang, Y. Yan, Y. Zheng, J. He, Y. Xie, G. He, Y. Wei, and X. Song Gene delivery with active targeting to ovarian cancer cells mediated by folate receptor α J. Biomed. Nanotechnol. 9 2013 833 844
25. Z. He, X. Zheng, X. Wu, X. Song, G. He, W. Wu, S. Yu, S. Mao, and Y. Wei Development of glycyrrhetinic acid-modified stealth cationic liposomes for gene delivery Int. J. Pharm. 397 2010 147 154
26. H.D. Han, L.S. Mangala, J.W. Lee, M.M.K. Shahzad, H.S. Kim, D. Shen, E.J. Nam, E.M. Mora, R.L. Stone, C. Lu, S.J. Lee, J.W. Roh, A.M. Nick, G. Lopez-Berestein, and A.K. Sood Targeted gene silencing using RGD-labeled chitosan nanoparticles Clin. Cancer Res. 16 2010 3910 3922
27. J. Halder, A.A. Kamat, C.N. Landen, L.Y. Han, S.K. Lutgendorf, Y.G. Lin, W.M. Merritt, N.B. Jennings, A. Chavez-Reyes, R.L. Coleman, D.M. Gershenson, R. Schmandt, S.W. Cole, G. Lopez-Berestein, and A.K. Sood Focal adhesion kinase targeting using in vivo short interfering RNA delivery in neutral liposomes for ovarian carcinoma therapy Clin. Cancer Res. 12 2006 4916 4924 (Pubitemid 44338579)
28. C.N. Landen, A. Chavez-Reyes, C. Bucana, R. Schmandt, M.T. Deavers, G. Lopez-Berestein, and A.K. Sood Therapeutic ephA2 gene targeting in vivo using neutral liposomal small interfering RNA delivery Cancer Res. 65 2005 6910 6918 (Pubitemid 41060730)
29. W. Shi, Q. Tang, X. Chen, P. Cheng, P. Jiang, X. Jing, X. Chen, P. Chen, Y. Wang, Y. Wei, and Y. Wen Antitumor and antimetastatic activities of vesicular stomatitis virus matrix protein in a murine model of breast cancer J. Mol. Med. 87 2009 493 506
30. S.M. Apte, D. Fan, J.J. Killion, and I.J. Fidler Targeting the platelet-derived growth factor receptor in antivascular therapy for human ovarian carcinoma Clin. Cancer Res. 10 2004 897 908 (Pubitemid 38198888)
31. L. Xu, J. Betker, H. Yin, and T.J. Anchordoquy Ligands located within a cholesterol domain enhance gene delivery to the target tissue J. Control. Release 160 2012 57 63
32. S. Dadashzadeh, N. Mirahmadi, M.H. Babaei, and A.M. Vali Peritoneal retention of liposomes: effects of lipid composition, PEG coating and liposome charge J. Control. Release 148 2010 177 186
33. C. Lonez, M. Vandenbranden, and J.-M. Ruysschaert Cationic lipids activate intracellular signaling pathways Adv. Drug Deliv. Rev. 64 2012 1749 1758
34. H. Lv, S. Zhang, B. Wang, S. Cui, and J. Yan Toxicity of cationic lipids and cationic polymers in gene delivery J. Control. Release 114 2006 100 109 (Pubitemid 44128621)
35. S. Fletcher, A. Ahmad, E. Perouzel, A. Heron, A.D. Miller, and M.R. Jorgensen In vivo studies of dialkynoyl analogues of DOTAP demonstrate improved gene transfer efficiency of cationic liposomes in mouse lung J. Med. Chem. 49 2006 349 357 (Pubitemid 43077347)
36. E. Kipps, D.S.P. Tan, and S.B. Kaye Meeting the challenge of ascites in ovarian cancer: new avenues for therapy and research Nat. Rev. Cancer 13 2013 273 282
37. Y. Chen, M. Chang, C. Huang, Y. Chiang, H. Lin, C. Chen, C. Hsieh, and W. Cheng Serous ovarian carcinoma patients with high alpha-folate receptor had reducing survival and cytotoxic chemo-response Mol. Oncol. 6 2012 360 369
38. L.C. Hartmann, G.L. Keeney, W.L. Lingle, T.J.H. Christianson, B. Varghese, D. Hillman, A.L. Oberg, and P.S. Low Folate receptor overexpression is associated with poor outcome in breast cancer Int. J. Cancer 121 2007 938 942 (Pubitemid 47101628)
39. M. Wu, W. Gunning, and M. Ratnam Expression of folate receptor type alpha in relation to cell type, malignancy, and differentiation in ovary, uterus, and cervix Cancer Epidemiol. Biomarkers Prev. 8 1999 775 782 (Pubitemid 29445014)
40. M. Figini, R. Ferri, D. Mezzanzanica, M. Bagnoli, E. Luison, S. Miotti, and S. Canevari Reversion of transformed phenotype in ovarian cancer cells by intracellular expression of anti folate receptor antibodies Gene Ther. 10 2003 1018 1025 (Pubitemid 36722492)
41. R. Agarwal, T. D'Souza, and P.J. Morin Claudin-3 and Claudin-4 expression in ovarian epithelial cells enhances invasion and is associated with increased matrix metalloproteinase-2 activity Cancer Res. 65 2005 7378 7385 (Pubitemid 41161271)
42. P.H. Thaker, L.Y. Han, A.A. Kamat, J.M. Arevalo, R. Takahashi, C. Lu, N.B. Jennings, G. Armaiz-Pena, J.A. Bankson, M. Ravoori, W.M. Merritt, Y.G. Lin, L.S. Mangala, T.J. Kim, R.L. Coleman, C.N. Landen, Y. Li, E. Felix, A.M. Sanguino, R.A. Newman, M. Lloyd, D.M. Gershenson, V. Kundra, G. Lopez-Berestein, S.K. Lutgendorf, S.W. Cole, and A.K. Sood Chronic stress promotes tumor growth and angiogenesis in a mouse model of ovarian carcinoma Nat. Med. 12 2006 939 944 (Pubitemid 44175146)
43. Charles River Laboratories Japan: BALB/c Nude Mouse Available at: http://www.criver.com/en-US/Pages/home.aspx 2013 (Accessed April 12, 2013)
44. S. Kawakami, Y. Ito, P. Charoensit, F. Yamashita, and M. Hashida Evaluation of proinflammatory cytokine production induced by linear and branched polyethylenimine/plasmid DNA complexes in mice J. Pharmacol. Exp. Ther. 317 2006 1382 1390 (Pubitemid 43764145)
45. C. Scholz, and E. Wagner Therapeutic plasmid DNA versus siRNA delivery: common and different tasks for synthetic carriers J. Control. Release 161 2011 554 565