Electrostatic interaction of tumor-targeting adenoviruses with aminoclay acquires enhanced infectivity to tumor cells inside the bladder and has better cytotoxic activity

References

• Adam L, Black PC, Kassouf W, et al. (2007). Adenoviral mediated interferon-alpha 2b gene therapy suppresses the pro-angiogenic effect of vascular endothelial growth factor in superficial bladder cancer. J Urol 177:1900–6.
   PubMed Web of Science ®Google Scholar
• Babu SR, Lakshmi VM, Huang GP, et al. (1996). Glucuronide conjugates of 4-aminobiphenyl and its N-hydroxy metabolites. pH stability and synthesis by human and dog liver. Biochem Pharmacol 51:1679–85.
   PubMed Web of Science ®Google Scholar
• Benedict WF, Tao Z, Kim CS, et al. (2004). Intravesical Ad-IFNalpha causes marked regression of human bladder cancer growing orthotopically in nude mice and overcomes resistance to IFN-alpha protein. Mol Ther 10:525–32.
   PubMed Web of Science ®Google Scholar
• Chester JD, Kennedy W, Hall GD, et al. (2003). Adenovirus-mediated gene therapy for bladder cancer: efficient gene delivery to normal and malignant human urothelial cells in vitro and ex vivo. Gene Ther 10:172–9.
   PubMed Web of Science ®Google Scholar
• Connor RJ, Engler H, Machemer T, et al. (2001). Identification of polyamides that enhance adenovirus-mediated gene expression in the urothelium. Gene Ther 8:41–8.
   PubMed Web of Science ®Google Scholar
• Croyle MA, Cheng X, Sandhu A, Wilson JM. (2001). Development of novel formulations that enhance adenoviral-mediated gene expression in the lung in vitro and in vivo. Mol Ther 4:22–8.
   PubMed Web of Science ®Google Scholar
• Douglas JT, Kim M, Sumerel LA, et al. (2001). Efficient oncolysis by a replicating adenovirus (ad) in vivo is critically dependent on tumor expression of primary ad receptors. Cancer Res 61:813–7.
   PubMed Web of Science ®Google Scholar
• El-Zawahry A, Lu P, White SJ, Voelkel-Johnson C. (2006). In vitro efficacy of AdTRAIL gene therapy of bladder cancer is enhanced by trichostatin A-mediated restoration of CAR expression and downregulation of cFLIP and Bcl-XL. Cancer Gene Ther 13:281–9.
   PubMed Web of Science ®Google Scholar
• Engler H, Anderson SC, Machemer TR, et al. (1999). Ethanol improves adenovirus-mediated gene transfer and expression to the bladder epithelium of rodents. Urology 53:1049–53.
   PubMed Web of Science ®Google Scholar
• Goh AR, Shin SP, Jung NR, et al. (2015). Low-dose cisplatin converts the tumor microenvironment into a permissive state for HSVtk-induced antitumor immunity in HPV16-related tonsillar carcinoma. Cancer Lett 356:743–50.
   PubMed Web of Science ®Google Scholar
• Gosnell H, Kasman LM, Potta T, et al. (2014). Polymer-enhanced delivery increases adenoviral gene expression in an orthotopic model of bladder cancer. J Control Release 176:35–43.
   PubMed Web of Science ®Google Scholar
• Kadlubar FF, Dooley KL, Teitel CH, et al. (1991). Frequency of urination and its effects on metabolism, pharmacokinetics, blood hemoglobin adduct formation, and liver and urinary bladder DNA adduct levels in beagle dogs given the carcinogen 4-aminobiphenyl. Cancer Res 51:4371–7.
   PubMed Web of Science ®Google Scholar
• Kadlubar FF, Miller JA, Miller EC. (1977). Hepatic microsomal N-glucuronidation and nucleic acid binding of N-hydroxy arylamines in relation to urinary bladder carcinogenesis. Cancer Res 37:805–14.
   PubMed Web of Science ®Google Scholar
• Kadlubar FF, Unruh LE, Flammang TJ, et al. (1981). Alteration of urinary levels of the carcinogen, N-hydroxy-2-naphthylamine, and its N-glucuronide in the rat by control of urinary pH, inhibition of metabolic sulfation, and changes in biliary excretion. Chem Biol Interact 33:129–47.
   PubMed Web of Science ®Google Scholar
• Kasman LM, Barua S, Lu P, et al. (2009). Polymer-enhanced adenoviral transduction of CAR-negative bladder cancer cells. Mol Pharmaceutics 6:1612–9.
   PubMed Web of Science ®Google Scholar
• Kim HS, Ku JH, Kim SJ, et al. (2016). Prognostic factors for recurrence and progression in Korean non-muscle-invasive bladder cancer patients: a retrospective, multi-institutional study. Yonsei Med J 57:855–64.
   PubMed Web of Science ®Google Scholar
• Kim SY, Lee SJ, Han HK, Lim SJ. (2017). Aminoclay as a highly effective cationic vehicle for enhancing adenovirus-mediated gene transfer through nanobiohybrid complex formation. Acta Biomater 49:521–30.
   PubMed Web of Science ®Google Scholar
• Kuball J, Wen SF, Leissner J, et al. (2002). Successful adenovirus-mediated wild-type p53 gene transfer in patients with bladder cancer by intravesical vector instillation. J Clin Oncol 20:957–65.
   PubMed Web of Science ®Google Scholar
• Li S, Wang F, Zhai Z, et al. (2017). Synergistic effect of bladder cancer-specific oncolytic adenovirus in combination with chemotherapy. Oncol Lett 14:2081–8.
   PubMed Web of Science ®Google Scholar
• Roberts DM, Nanda A, Havenga MJ, et al. (2006). Hexon-chimaeric adenovirus serotype 5 vectors circumvent pre-existing anti-vector immunity. Nature 441:239–43.
   PubMed Web of Science ®Google Scholar
• Roelvink PW, Lizonova A, Lee JG, et al. (1998). The coxsackievirus-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. J Virol 72:7909–15.
   PubMed Web of Science ®Google Scholar
• Rothman N, Talaska G, Hayes RB, et al. (1997). Acidic urine pH is associated with elevated levels of free urinary benzidine and N-acetylbenzidine and urothelial cell DNA adducts in exposed workers. Cancer Epidemiol Biomarkers Prev 6:1039–42.
   PubMed Web of Science ®Google Scholar
• Shieh GS, Shiau AL, Yo YT, et al. (2006). Low-dose etoposide enhances telomerase-dependent adenovirus-mediated cytosine deaminase gene therapy through augmentation of adenoviral infection and transgene expression in a syngeneic bladder tumor model. Cancer Res 66:9957–66.
   PubMed Web of Science ®Google Scholar
• Shore ND, Boorjian SA, Canter DJ, et al. (2017). Intravesical rAd-IFNalpha/Syn3 for patients with high-grade, Bacillus Calmette-Guerin-refractory or relapsed non-muscle-invasive bladder cancer: a phase II randomized study. J Clin Oncol 35:3410–6.
   PubMed Web of Science ®Google Scholar
• Siegel R, Naishadham D, Jemal A. (2013). Cancer statistics, 2013. CA Cancer J Clin 63:11–30.
   PubMed Web of Science ®Google Scholar
• Tomita K, Sakurai F, Tachibana M, Mizuguchi H. (2012). Correlation between adenovirus-neutralizing antibody titer and adenovirus vector-mediated transduction efficiency following intratumoral injection. Anticancer Res 32:1145–52.
   PubMed Web of Science ®Google Scholar
• Watanabe T, Shinohara N, Sazawa A, et al. (2000). An improved intravesical model using human bladder cancer cell lines to optimize gene and other therapies. Cancer Gene Ther 7:1575–80.
   PubMed Web of Science ®Google Scholar
• Werthman PE, Drazan KE, Rosenthal JT, et al. (1996). Adenoviral-p53 gene transfer to orthotopic and peritoneal murine bladder cancer. J Urol 155:753–6.
   PubMed Web of Science ®Google Scholar
• Yamashita M, Rosser CJ, Zhou JH, et al. (2002). Syn3 provides high levels of intravesical adenoviral-mediated gene transfer for gene therapy of genetically altered urothelium and superficial bladder cancer. Cancer Gene Ther 9:687–91.
   PubMed Web of Science ®Google Scholar
• Young JF, Kadlubar FF. (1982). A pharmacokinetic model to predict exposure of the bladder epithelium to urinary N-hydroxyarylamine carcinogens as a function of urine pH, voiding interval, and resorption. Drug Metab Dispos 10:641–4.
   PubMed Web of Science ®Google Scholar
• Zhu HJ, Zhang ZQ, Zeng XF, et al. (2004). Cloning and analysis of human UroplakinII promoter and its application for gene therapy in bladder cancer. Cancer Gene Ther 11:263–72.
   PubMed Web of Science ®Google Scholar