Suppression of tumor growth in lung cancer xenograft model mice by poly(sorbitol-co-PEI)-mediated delivery of osteopontin siRNA

European Journal of Pharmaceutics and Biopharmaceutics

Volumn 94, Issue , 2015, Pages 450-462

  Cho, Won Young ^a   Hong, Seong Ho ^a   Singh, Bijay ^a   Islam, Mohammad Ariful ^a,b,c   Lee, Somin ^a   Lee, Ah Young ^a   Gankhuyag, Nomundelger ^a   Kim, Ji Eun ^a   Yu, Kyeong Nam ^a   Kim, Kwang Ho ^d   Park, Young Chan ^d   Cho, Chong Su ^a   Cho, Myung Haing ^a,e  

^a Seoul National University   (South Korea)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d Croen Research   (South Korea)

^e Seoul National University   (South Korea)

Author keywords

Lung cancer gene therapy; Osteopontin; Polysorbitol based transporter; siRNA

Indexed keywords

CISPLATIN; OSTEOPONTIN; POLY(SORBITOL CO POLYETHYLENEIMINE); POLYETHYLENEIMINE DERIVATIVE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; DRUG CARRIER; POLYETHYLENEIMINE; SORBITOL; SPP1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; CYTOTOXICITY; DRUG TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; DRUG SCREENING; GENE EXPRESSION; GENE SILENCING; GENE TRANSFER; GENETICS; LUNG NEOPLASMS; NUDE MOUSE; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; DRUG CARRIERS; GENE EXPRESSION; GENE SILENCING; GENE TRANSFER TECHNIQUES; HUMANS; LUNG NEOPLASMS; MALE; MICE, INBRED BALB C; MICE, NUDE; OSTEOPONTIN; POLYETHYLENEIMINE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SORBITOL; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84936951419     PISSN: 09396411     EISSN: 18733441     Source Type: Journal    
DOI: 10.1016/j.ejpb.2015.06.017     Document Type: Article

References (57)

1. P. Goldstraw, D. Ball, J.R. Jett, T.L. Chevalier, E. Lim, A.G. Nicholson, and F.A. Shepherd Non small-cell lung cancer Lancet Oncol. 378 2011 1727 1740
2. J.R. Molina, P. Yang, S.D. Cassivi, S.E. Schild, and A.A. Adjei Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship Mayo Clin. Proc. 83 2008 584 594
3. J. Zhang, K. Takahashi, F. Takahashi, K. Shimizu, F. Ohshita, Y. Kameda, K. Maeda, K. Nishio, and Y. Fukuchi Differential osteopontin expression in lung cancer Cancer Lett. 171 2001 215 222
4. Z. Hu, D. Lin, J. Yuan, T. Xiao, H. Zhang, W. Sun, N. Han, Y. Ma, X. Di, M. Gao, J. Ma, J. Zhang, S. Cheng, and Y. Gao Overexpression of osteopontin is associated with more aggressive phenotypes in human non-small cell lung cancer Clin. Cancer Res. 11 2005 4646 4652
5. Y.S. Chang, H.J. Kim, J. Chang, C.M. Ahn, S.K. Kim, and S.K. Kim Elevated circulating level of osteopontin is associated with advanced disease state of non-small cell lung cancer Lung Cancer 57 2007 373 380
6. B. Zhao, T. Sun, F. Meng, A. Qu, C. Li, H. Shen, Y. Jin, and W. Li Osteopontin as a potential biomarker of proliferation and invasiveness for lung cancer J. Cancer Res. Clin. Oncol. 137 2011 1061 1070
7. J. Wu, P. Pungaliya, E. Kraynov, and B. Bates Identification and quantification of osteopontin splice variants in the plasma of lung cancer patients using immunoaffinity capture and targeted mass spectrometry Biomarkers 17 2012 125 133
8. S.H. Chang, A. Minai-Tehrani, J.Y. Shin, S. Park, J.E. Kim, K.N. Yu, S.H. Hong, C.M. Hong, K.H. Lee, and G.R. Beck Beclin1-induced autophagy abrogates radioresistance of lung cancer cells by suppressing osteopontin J. Radiat. Res. 53 2012 422 432
9. A. Minai-Tehrani, S.H. Chang, J.T. Kwon, S.K. Hwang, J.E. Kim, J.Y. Shin, K.N. Yu, S.J. Park, H.L. Jiang, J.H. Kim, S.H. Hong, B. Kang, D. Kim, C.H. Chae, K.H. Lee, G.R. Beck, and M.H. Cho Aerosol delivery of lentivirus-mediated O-glycosylation mutant osteopontin suppresses lung tumorigenesis in K-ras (LA1) mice Cell Oncol. 36 2013 15 26
10. K.N. Yu, A. Minai-Tehrani, S.H. Chang, S.K. Hwang, S.H. Hong, J.E. Kim, J.Y. Shin, S.J. Park, J.H. Kim, J.T. Kwon, H.L. Jiang, B. Kang, D. Kim, C.H. Chae, K.H. Lee, T.J. Yoon, G.R. Beck, and M.H. Cho Aerosol delivery of small hairpin osteopontin blocks pulmonary metastasis of breast cancer in mice PLoS ONE 5 2010 e15623
11. T. Merdan, J. Kopecek, and T. Kissel Prospects for cationic polymers in gene and oligonucleotide therapy against cancer Adv. Drug Deliv. Rev. 54 2002 715 758
12. K.F. Pirollo, and E.H. Chang Targeted delivery of small interfering RNA: approaching effective cancer therapies Cancer Res. 68 2008 1247 1250
13. A. Minai-Tehrani, H.L. Jiang, Y.K. Kim, Y.S. Chung, K.N. Yu, J.E. Kim, J.Y. Shin, S.H. Hong, J.H. Lee, H.J. Kim, S.H. Chang, S. Park, B.N. Kang, C.S. Cho, and M.H. Cho Suppression of tumor growth in xenograft model mice by small interfering RNA targeting osteopontin delivery using biocompatible poly(amino ester) Int. J. Pharm. 431 2012 197 203
14. S.H. Hong, A. Minai-Tehrani, S.H. Chang, H.L. Jiang, S. Lee, A.Y. Lee, H.W. Seo, C. Chae, G.R. Beck Jr., and M.H. Cho Knockdown of the sodium-dependent phosphate co-transporter 2b (NPT2b) suppresses lung tumorigenesis PLoS ONE 8 2013 e77121
15. S.H. Hong, S.J. Park, S. Lee, C.S. Cho, and M.H. Cho Aerosol gene delivery using viral vectors and cationic carriers for in vivo lung cancer therapy Expert Opin. Drug Deliv. 12 2015 977 991
16. M.A. Islam, J.Y. Shin, C.H. Yun, C.S. Cho, H.W. Seo, C. Chae, and M.H. Cho The effect of RNAi silencing of p62 using an osmotic polysorbitol transporter on autophagy and tumorigenesis in lungs of K-rasLA1 mice Biomaterials 35 2014 1584 1596
17. Q.P. Luu, J.Y. Shin, Y.K. Kim, M.A. Islam, S.K. Kang, M.H. Cho, Y.J. Choi, and C.S. Cho High gene transfer by the osmotic polysorbitol-mediated transporter through the selective caveolae endocytic pathway Mol. Pharm. 9 2012 2206 2218
18. M.A. Islam, C.H. Yun, Y.J. Choi, J.Y. Shin, R. Arote, H.L. Jiang, S.K. Kang, J.W. Nah, I.K. Park, M.H. Cho, and C.S. Cho Accelerated gene transfer through a polysorbitol-based transporter mechanism Biomaterials 32 2011 9908 9924
19. B.U. Klein, S. Werth, S. Abuharbeid, F. Czubayko, and A. Aigner RNAi-mediated gene-targeting through systemic application of polyethylenimine (PEI)-complexed siRNA in vivo Gene Ther. 12 2005 461 466
20. M. Ahmed, R. Behera, G. Chakraborty, S. Jain, V. Kumar, P. Sharma, A. Bulbule, S. Kale, S. Kumar, R. Mishra, R. Raja, S. Saraswati, R. Kaur, G. Soundararajan, D. Kumar, D. Thorat, M. Sanyal, A. Ramdasi, P. Ghosh, and G.C. Kundu Osteopontin: a potentially important therapeutic target in cancer Expert Opin. Ther. Targets 15 2011 1113 1126
21. X.L. Wu, K.J. Lin, A.P. Bai, W.X. Wang, X.K. Meng, X.L. Su, M.X. Hou, P.D. Dong, J.J. Zhang, Z.Y. Wang, and L. Shi Osteopontin knockdown suppresses the growth and angiogenesis of colon cancer cells World J. Gastroenterol. 20 2014 10440 10448
22. L.A. Shevde, R.S. Samant, J.C. Paik, B.J. Metge, A.F. Chambers, G. Casey, A.R. Frost, and D.R. Welch Osteopontin knockdown suppresses tumorigenicity of human metastatic breast carcinoma, MDA-MB-435 Clin. Exp. Metastasis 23 2006 123 133
23. D.X. Cao, Z.J. Li, X.O. Jiang, Y.L. Lum, E. Khin, N.P. Lee, G.H. Wu, and J.M. Luk Osteopontin as potential biomarker and therapeutic target in gastric and liver cancers World J. Gastroenterol. 18 2012 3923 3930
24. S. Akhtar, and I.F. Benter Nonviral delivery of synthetic siRNAs in vivo J. Clin. Invest. 117 2007 3623 3632
25. L. Liu, S. Wang, B. Shan, M. Sang, S. Liu, and G. Wang Advances in viral-vector systemic cytokine gene therapy against cancer Vaccine 28 2010 3883 3887
26. J.Q. Yin, J. Gao, R. Shao, W.N. Tian, J. Wang, and Y. Wan siRNA agents inhibit oncogene expression and attenuate human tumor cell growth J. Exp. Ther. Oncol. 3 2003 194 204
27. A. Aigner Delivery systems for the direct application of siRNAs to induce RNA interference (RNAi) in vivo J. Biomed. Biotechnol. 2006 2006 71659
28. D. Fischer, T. Bieber, Y. Li, H.P. Elsässer, and T. Kissel A novel non-viral vector for DNA delivery based on low molecular weight, branched polyethylenimine: effect of molecular weight on transfection efficiency and cytotoxicity Pharm. Res. 16 1999 1273 1279
29. A. Kichler Gene transfer with modified polyethylenimines J. Gene Med. 6 2004 S3 S10
30. M. Ma, F. Li, Z.F. Yuan, and R.X. Zhuo Influence of hydroxyl groups on the biological properties of cationic polymethacrylates as gene vectors Acta Biomater. 6 2010 2658 2665
31. Y. Liu, and T.M. Reineke Hydroxyl stereochemistry and amine number within poly(glycoamidoamine)s affect intracellular DNA delivery J. Am. Chem. Soc. 127 2005 3004 3015
32. N.G. Schipper, K.M. Vårum, and P. Artursson Chitosans as absorption enhancers for poorly absorbable drugs. 1: Influence of molecular weight and degree of acetylation on drug transport across human intestinal epithelial (Caco-2) cells Pharm. Res. 13 1996 1686 1692
33. R. Arote, T.H. Kim, Y.K. Kim, S.K. Hwang, H.L. Jiang, H.H. Song, J.W. Nah, M.H. Cho, and C.S. Cho A biodegradable poly(ester amine) based on polycaprolactone and polyethylenimine as a gene carrier Biomaterials 28 2007 735 744
34. K.A. Mislick, and J.D. Baldeschwieler Evidence for the role of proteoglycans in cation-mediated gene transfer Proc. Natl. Acad. Sci. U S A. 1996 12349 12354
35. W.T. Godbey, K.K. Wu, and A.G. Mikos Poly(ethylenimine) and its role in gene delivery J. Control. Release 60 1999 149 160
36. R. Kircheis, L. Wightman, and E. Wagner Design and gene delivery activity of modified polyethylenimines Adv. Drug Deliv. Rev. 53 2001 341 358
37. M. Sioud On the delivery of small interfering RNAs into mammalian cells Expert Opin. Drug Deliv. 2 2005 639 651
38. R. Zhang, L. Zhang, and W. Yu Genome-wide expression of non-coding RNA and global chromatin modification Acta Biochim. Biophys. 44 2012 40 47
39. Y. Wang, Z. Xu, S. Guo, L. Zhang, A. Sharma, G.P. Robertson, and L. Huang Intravenous delivery of siRNA targeting CD47 effectively inhibits melanoma tumor growth and lung metastasis Mol. Ther. 21 2013 1919 1929
40. Y. Zhang, L. Li, J. Yu, D. Zhu, Y. Zhang, X. Li, H. Gu, C.Y. Zhang, and K. Zen Microvesicle-mediated delivery of transforming growth factor β1 siRNA for the suppression of tumor growth in mice Biomaterials 35 2014 4390 4400
41. S.D. Li, S. Chono, and L. Huang Efficient oncogene silencing and metastasis inhibition via systemic delivery of siRNA Mol. Ther. 16 2008 942 946
42. I.E. Smith, M.E. O'Brien, D.C. Talbot, M.C. Nicolson, J.L. Mansi, T.F. Hickish, A. Norton, and S. Ashley Duration of chemotherapy in advanced non-small-cell lung cancer: a randomized trial of three versus six courses of mitomycin, vinblastine, and cisplatin J. Clin. Oncol. 19 2001 1336 1343
43. R. Cortés, M. Tarrado-Castellarnau, D. Talancón, C. López, W. Link, D. Ruiz, J.J. Centelles, J. Quirante, and M. Cascante A novel cyclometallated Pt(II)-ferrocene complex induces nuclear FOXO3a localization and apoptosis and synergizes with cisplatin to inhibit lung cancer cell proliferation Metallomics 6 2014 622 633
44. M. Thomas, J.J. Lu, J. Chen, and A.M. Klibanov Non-viral siRNA delivery to the lung Adv. Drug Deliver. Rev. 59 2007 124 133
45. C.R. Drake, A. Aissaoui, O. Argyros, J.M. Serginson, B.D. Monnery, M. Thanou, J.H. Steinke, and A.D. Miller Bioresponsive small molecule polyamines as noncytotoxic alternative to polyethylenimine Mol. Pharm. 7 2010 2040 2055
46. Y. Matsumura, and H. Maeda A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs Cancer Res. 46 1986 6387 6392
47. R. Duncan, Y.N. Sat-Klopsch, A.M. Burger, M.C. Bibby, H.H. Fiebig, and E.A. Sausville Validation of tumour models for use in anticancer nanomedicine evaluation: the EPR effect and cathepsin B-mediated drug release rate Cancer Chemother. Pharmacol. 72 2013 417 427
48. H. Maeda, J. Wu, T. Sawa, Y. Matsumura, and K. Hori Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review J. Control. Release 65 2000 271 284
49. H. Maeda, and Y. Matsumura EPR effect based drug design and clinical outlook for enhanced cancer chemotherapy Adv. Drug Deliv. Rev. 63 2011 129 130
50. L.F. Brown, B. Berse, L. Van de Water, A. Papadopoulos-Sergiou, C.A. Perruzzi, E.J. Manseau, H.F. Dvorak, and D.R. Senger Expression and distribution of osteopontin in human tissues: widespread association with luminal epithelial surfaces Mol. Biol. Cell 3 1992 1169 1180
51. K. Yoon, R. Buenaga, and G.A. Rodan Tissue specificity and developmental expression of rat osteopontin Biochem. Biophys. Res. Commun. 148 1987 1129 1136
52. T. Kubota, Q. Zhang, J.L. Wrana, R. Ber, J.E. Aubin, W.T. Butler, and J. Sodek Multiple forms of SppI (secreted phosphoprotein, osteopontin) synthesized by normal and transformed rat bone cell populations: regulation by TGF-beta Biochem. Biophys. Res. Commun. 162 1989 1453 1459
53. A.F. Chambers, S.M. Wilson, N. Kerkvliet, F.P. O'Malley, J.F. Harris, and A.G. Casson Osteopontin expression in lung cancer Lung Cancer 15 1996 311 323
54. N. Shijubo, T. Uede, S. Kon, M. Maeda, T. Segawa, A. Imada, M. Hirasawa, and S. Abe Vascular endothelial growth factor and osteopontin in stage I lung adenocarcinoma Am. J. Respir. Crit. Care Med. 160 1999 1269 1273
55. Y.J. Cheng, H.S. Jiang, S.L. Hsu, L.C. Lin, C.L. Wu, V.K. Ghanta, and C.M. Hsueh XIAP-mediated protection of H460 lung cancer cells against cisplatin Eur. J. Pharmacol. 627 2010 75 84
56. E.I. Behrend, A.M. Craig, S.M. Wilson, D.T. Denhardt, and A.F. Chambers Reduced malignancy of ras-transformed NIH 3T3 cells expressing antisense osteopontin RNA Cancer Res. 54 1999 832 837
57. H.A. Gardner, B. Berse, and D.R. Senger Specific reduction in osteopontin synthesis by antisense RNA inhibits the tumorigenicity of transformed Rat1 fibroblasts Oncogene 9 1994 2321 2326