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Review

The current status of gene therapy in bladder cancer

ORCID Icon, , ORCID Icon & ORCID Icon
Pages 531-543 | Received 13 Dec 2022, Accepted 12 Apr 2023, Published online: 25 Apr 2023

References

  • US Food and Drug Administration. What is gene therapy? 07/2018 [10/2022]. Available from: https://www.fda.gov/vaccines-blood-biologics/cellular-gene-therapy-products/what-gene-therapy.
  • Linden R. Gene therapy: what it is, what it is not and what it will be. Estud Av. 2010;24(70):31–69.
  • Papanikolaou E, Bosio A. The promise and the hope of gene therapy. Frontiers in Genome Ed. 2021;3. DOI:10.3389/fgeed.2021.618346
  • Friedmann T, Roblin R. Gene therapy for human genetic disease? Science. 1972;175(4025):949–955. PubMed PMID: 5061866. DOI:10.1126/science.175.4025.949
  • Wirth T, Parker N, Ylä-Herttuala S. History of gene therapy. Gene. 2013;525(2):162–169.
  • Griffith F. The significance of pneumococcal types. J Hyg (Lond). 1928;27(2):113–159. PubMed PMID: 20474956; PubMed Central PMCID: PMC2167760. DOI:10.1017/s0022172400031879
  • Avery OT, Macleod CM, McCarty M. Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus Type Iii. J Exp Med. 1944;79(2):137–158. PubMed PMID: 19871359; PubMed Central PMCID: PMC2135445. DOI:10.1084/jem.79.2.137
  • Tatum EL, Lederberg J. Gene Recombination in the Bacterium Escherichia coli. J Bacteriol. 1947;53(6):673–684. PubMed PMID: 16561324; PubMed Central PMCID: PMC518375. DOI:10.1128/jb.53.6.673-684.1947
  • Zinder ND, Lederberg J. Genetic exchange in Salmonella. J Bacteriol. 1952;64(5):679–699. PubMed PMID: 12999698; PubMed Central PMCID: PMC169409. DOI:10.1128/jb.64.5.679-699.1952
  • Temin HM. Mixed infection with two types of Rous sarcoma virus. Virology. 1961;13:158–163. PubMed PMID: 13775833. DOI:10.1016/0042-6822(61)90049-6
  • Rogers S, Pfuderer P. Use of viruses as carriers of added genetic information. Nature. 1968;219(5155):749–751.
  • Rogers S, Lowenthal A, Terheggen HG, et al. Induction of arginase activity with the Shope papilloma virus in tissue culture cells from an argininemic patient. J Exp Med. 1973;137(4):1091–1096. PubMed PMID: 4348278; PubMed Central PMCID: PMC2139227 DOI:10.1084/jem.137.4.1091
  • Terheggen HG, Lowenthal A, Lavinha F, et al. Unsuccessful trial of gene replacement in arginase deficiency. Z Kinderheilkd. 1975;119(1):1–3. PubMed PMID: 164740 DOI:10.1007/BF00464689
  • Blaese RM, Culver KW, Miller AD, et al. T lymphocyte-directed gene therapy for ADA- SCID: initial trial results after 4 years. Science. 1995;270(5235):475–480. PubMed PMID: 7570001 DOI:10.1126/science.270.5235.475
  • Stolberg SG. The biotech death of Jesse Gelsinger. N Y Times Mag. 1999;136-40:49–50. PubMed PMID: 11647737.
  • Fehse B, Roeder I. Insertional mutagenesis and clonal dominance: biological and statistical considerations. Gene Ther. 2008;15(2):143–153. Epub 20071101. PubMed PMID: 17972922. DOI:10.1038/sj.gt.3303052
  • Howe SJ, Mansour MR, Schwarzwaelder K, et al. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J Clin Invest. 2008;118(9):3143–3150.
  • Wang D, Tai PWL, Gao G. Adeno-associated virus vector as a platform for gene therapy delivery. Nat Rev Drug Discov. 2019;18(5):358–378.
  • Bulcha JT, Wang Y, Ma H, et al. Viral vector platforms within the gene therapy landscape. Signal Transduct Target Ther. 2021;6(1). DOI:10.1038/s41392-021-00487-6
  • Hedman M, Muona K, Hedman A, et al. Eight-year safety follow-up of coronary artery disease patients after local intracoronary VEGF gene transfer. Gene Ther. 2009;16(5):629–634. Epub 20090212 Epub 20090212 DOI:10.1038/gt.2009.4
  • Muona K, Makinen K, Hedman M, et al. 10-year safety follow-up in patients with local VEGF gene transfer to ischemic lower limb. Gene Ther. 2012;19(4):392–395. Epub 20110721PubMed PMID: 21776026 DOI:10.1038/gt.2011.109
  • Pich O, Muinos F, Lolkema MP, et al. The mutational footprints of cancer therapies. Nat Genet. 2019;51(12):1732–1740. Epub 20191118 Epub 20191118 DOI:10.1038/s41588-019-0525-5
  • Wu C, Lu Y. Inclusion of high molecular weight dextran in calcium phosphate-mediated transfection significantly improves gene transfer efficiency. Cell Mol Biol (Noisy-le-Grand). 2007;53(4): 67–74. Epub 20070515. PubMed PMID: 17531163; PubMed Central PMCID: PMC2830788.
  • Dass CR. Lipoplex-mediated delivery of nucleic acids: factors affecting in vivo transfection. J Mol Med (Berl). 2004;82(9):579–591. Epub 20040623 Epub 20040623. DOI:10.1007/s00109-004-0558-8
  • Herweijer H, Wolff JA. Gene therapy progress and prospects: hydrodynamic gene delivery. Gene Ther. 2007;14(2):99–107. Epub 20061130 Epub 20061130. DOI:10.1038/sj.gt.3302891
  • Favard C, Dean DS, Rols M-P. Electrotransfer as a non viral method of gene delivery. curr Gene Ther. 2007;7(1):67–77. PubMed PMID: 17305529. DOI:10.2174/156652307779940207
  • Chen YH, Keiser MS, Davidson BL. Viral vectors for gene transfer. Curr Protoc Mouse Biol. 2018;8(4):e58. Epub 20181128; PubMed PMID: 30485696. DOI:10.1002/cpmo.58
  • Nathwani AC, Davidoff AM, Linch DC. A review of gene therapy for haematological disorders. Br J Haematol. 2005;128(1):3–17. PubMed PMID: 15606545. DOI:10.1111/j.1365-2141.2004.05231.x
  • Goncalves GAR, Paiva RMA. Gene therapy: advances, challenges and perspectives. Einstein (Sao Paulo). Einstein (SaoPaulo). 2017;15(3):369–375. PubMed PMID: 29091160; PubMed Central PMCID: PMC5823056. DOI:10.1590/S1679-45082017RB4024
  • Sanvicens N, Marco MP. Multifunctional nanoparticles–properties and prospects for their use in human medicine. Trends Biotechnol. 2008;26(8):425–433. PubMed PMID: 18514941. DOI:10.1016/j.tibtech.2008.04.005
  • Pardridge WM. Blood–brain barrier delivery of protein and non-viral gene therapeutics with molecular Trojan horses. J Controlled Release. 2007;122(3):345–348. Epub 20070406; PubMed PMID: 17512078; PubMed Central PMCID: PMC2701689. DOI:10.1016/j.jconrel.2007.04.001
  • Hauser O, Prieschl-Grassauer E, Salmons B. Encapsulated, genetically modified cells producing in vivo therapeutics. Curr Opin Mol Ther. 2004;6(4): 412–420. PubMed PMID: 15468600.
  • Arabi F, Mansouri V, Ahmadbeigi N. Gene therapy clinical trials, where do we go? An overview. Biomed Pharmacother. 2022;153:113324. Epub 20220629 Epub 20220629. DOI:10.1016/j.biopha.2022.113324
  • Razi Soofiyani S, Baradaran B, Lotfipour F, et al. Gene therapy, early promises, subsequent problems, and recent breakthroughs. Adv Pharm Bull. 2013;3(2):249–255. Epub 20130820 Epub 20130820 DOI:10.5681/apb.2013.041
  • Irie A. Advances in gene therapy for bladder cancer. Curr Gene Ther. 2003;3(1):1–11. PubMed PMID: 12553531. DOI:10.2174/1566523033347499
  • Byrne D, Daly C, Nicamhlaoibh R, et al. Use of ribozymes and antisense oligodeoxynucleotides to investigate mechanisms of drug resistance. Cytotechnology. 1998;27(1–3):113–136. PubMed PMID: 19002787; PubMed Central PMCID: PMC3449559 DOI:10.1023/A:1008052401952
  • Kashani-Sabet M, Funato T, Tone T, et al. Reversal of the malignant phenotype by an anti-ras ribozyme. Antisense Res Dev. 1992;2(1):3–15. PubMed PMID: 1422085 DOI:10.1089/ard.1992.2.3
  • Mizutani Y, Fukumoto M, Bonavida B, et al. Enhancement of sensitivity of urinary bladder tumor cells to cisplatin by c-myc antisense oligonucleotide. Cancer. 1994;74(9):2546–2554. PubMed PMID: 7923012 DOI:10.1002/1097-0142(19941101)74:9<2546:aid-cncr2820740924>3.0.co;2-y
  • Irie A, Kashani-Sabet M, Scanlon KJ, et al. Hammerhead ribozymes as therapeutic agents for bladder cancer. Mol Urol. 2000;4(2):61–66. PubMed PMID: 12006244 DOI:10.1089/10915360050138602
  • Yang C, Cirielli C, Capogrossi MC, et al. Adenovirus-mediated wild-type p53 expression induces apoptosis and suppresses tumorigenesis of prostatic tumor cells. Cancer Res. 1995;55(19):4210–4213. PubMed PMID: 7671222.
  • Sugrue MM, Shin DY, Lee SW, et al. Wild-type p53 triggers a rapid senescence program in human tumor cells lacking functional p53. Proc Natl Acad Sci U S A. 1997;94(18):9648–9653. PubMed PMID: 9275177; PubMed Central PMCID: PMC23243 DOI:10.1073/pnas.94.18.9648
  • Irie A, Matsumoto K, Anderegg B, et al. Growth inhibition efficacy of an adenovirus expressing dual therapeutic genes, wild-type p53, and anti-erbB2 ribozyme, against human bladder cancer cells. Cancer Gene Ther. 2006;13(3):298–305. PubMed PMID: 16110311 DOI:10.1038/sj.cgt.7700892
  • Xu HJ, Zhou Y, Seigne J, et al. Enhanced tumor suppressor gene therapy via replication-deficient adenovirus vectors expressing an N-terminal truncated retinoblastoma protein. Cancer Res. 1996;56(10):2245–2249. PubMed PMID: 8625292.
  • Pan JG, Zhou X, Luo R, et al. The adeno-associated virus-mediated HSV-TK/GCV suicide system: a potential strategy for the treatment of bladder carcinoma. Med Oncol. 2012;29(3):1938–1947. Epub 20111020 Epub 20111020 DOI:10.1007/s12032-011-0091-x
  • Ries S, Korn WM. ONYX-015: mechanisms of action and clinical potential of a replication-selective adenovirus. Br J Cancer. 2002;86(1):5–11. PubMed PMID: 11857003; PubMed Central PMCID: PMC2746528. DOI:10.1038/sj.bjc.6600006
  • Nemunaitis J, Khuri F, Ganly I, et al. Phase II trial of intratumoral administration of ONYX-015, a replication-selective adenovirus, in patients with refractory head and neck cancer. J Clin Oncol. 2001;19(2):289–298. PubMed PMID: 11208818 DOI:10.1200/JCO.2001.19.2.289
  • Ramesh N, Ge Y, Ennist DL, et al. CG0070, a conditionally replicating granulocyte macrophage colony-stimulating factor–armed oncolytic adenovirus for the treatment of bladder cancer. Clin Cancer Res. 2006;12(1):305–313. PubMed PMID: 16397056 DOI:10.1158/1078-0432.CCR-05-1059
  • Jakubczak JL, Ryan P, Gorziglia M, et al. An oncolytic adenovirus selective for retinoblastoma tumor suppressor protein pathway-defective tumors: dependence on E1A, the E2F-1 promoter, and viral replication for selectivity and efficacy. Cancer Res. 2003;63(7):1490–1499. PubMed PMID: 12670895.
  • Chen L, Chen D, Block E, et al. Eradication of murine bladder carcinoma by intratumor injection of a bicistronic adenoviral vector carrying cDnas for the IL-12 heterodimer and its inhibition by the IL-12 p40 subunit homodimer. J Immunol. 1997;159(1):351–359. PubMed PMID: 9200473. DOI:10.4049/jimmunol.159.1.351
  • Hashimura T, Ueda T, Hiura M, et al. Gene therapy by in vivo interferon-gamma gene transfer to murine bladder tumor. Hinyokika Kiyo. 1997;43(11):809–813. PubMed PMID: 9436027.
  • Horiguchi Y, Larchian WA, Kaplinsky R, et al. Intravesical liposome-mediated interleukin-2 gene therapy in orthotopic murine bladder cancer model. Gene Ther. 2000;7(10):844–851. PubMed PMID: 10845722 DOI:10.1038/sj.gt.3301157
  • Bochner BH. Gene therapy in bladder cancer. Curr Opin Urol. 2008;18(5):519–523. PubMed PMID: 18670278. DOI:10.1097/MOU.0b013e32830b86e3
  • Nickel JC, Downey J, Morales A, et al. Relative efficacy of various exogenous glycosaminoglycans in providing a bladder surface permeability barrier. J Urol. 1998;160(2):612–614. PubMed PMID: 9679938. DOI:10.1016/S0022-5347(01)62968-9
  • Sabichi A, Keyhani A, Tanaka N, et al. Characterization of a panel of cell lines derived from urothelial neoplasms: genetic alterations, growth in vivo and the relationship of adenoviral mediated gene transfer to coxsackie adenovirus receptor expression. J Urol. 2006;175(3 Pt 1):1133–1137. PubMed PMID: 16469639 DOI:10.1016/S0022-5347(05)00323-X
  • Buscarini M, Quek ML, Gilliam-Hegarich S, et al. Adenoviral receptor expression of normal bladder and transitional cell carcinoma of the bladder. Urol Int. 2007;78(2):160–166. PubMed PMID: 17293658 DOI:10.1159/000098076
  • Li Y, Pong RC, Bergelson JM, et al. Loss of adenoviral receptor expression in human bladder cancer cells: a potential impact on the efficacy of gene therapy. Cancer Res. 1999;59(2):325–330. PubMed PMID: 9927041.
  • Sachs MD, Ramamurthy M, Poel H, et al. Histone deacetylase inhibitors upregulate expression of the coxsackie adenovirus receptor (CAR) preferentially in bladder cancer cells. Cancer Gene Ther. 2004;11(7):477–486. PubMed PMID: 15118762 DOI:10.1038/sj.cgt.7700726
  • Lee CT, Seol JY, Park KH, et al. Differential effects of adenovirus-p16 on bladder cancer cell lines can be overcome by the addition of butyrate. Clin Cancer Res. 2001;7(1):210–214. PubMed PMID: 11205911.
  • Segura-Pacheco B, Avalos B, Rangel E, et al. HDAC inhibitor valproic acid upregulates CAR in vitro and in vivo. Genet Vaccines Ther. 2007;5:10. Epub 20070924 Epub 20070924. DOI:10.1186/1479-0556-5-10
  • Siemens DR, Austin JC, See WA, et al. Evaluation of gene transfer efficiency by viral vectors to murine bladder epithelium. J Urol. 2001;165(2):667–671. PubMed PMID: 11176455 DOI:10.1097/00005392-200102000-00091
  • Grossman HB, Liebert M, Lee IW, et al. Decreased connexin expression and intercellular communication in human bladder cancer cells. Cancer Res. 1994;54(11):3062–3065. PubMed PMID: 8187096.
  • Tanaka M, Fraizer GC, De La Cerda J, et al. Connexin 26 enhances the bystander effect in HSVtk/GCV gene therapy for human bladder cancer by adenovirus/PLL/DNA gene delivery. Gene Ther. 2001;8(2):139–148. PubMed PMID: 11313783 DOI:10.1038/sj.gt.3301367
  • Badalament RA, Franklin GL, Page CM, et al. Enhancement of bacillus Calmette-Guerin attachment to the urothelium by removal of the rabbit bladder mucin layer. J Urol. 1992;147(2):482–485. PubMed PMID: 1732628 DOI:10.1016/s0022-5347(17)37284-1
  • Engler H, Anderson SC, Machemer TR, et al. Ethanol improves adenovirus-mediated gene transfer and expression to the bladder epithelium of rodents. Urology. 1999;53(5):1049–1053. PubMed PMID: 10223504 DOI:10.1016/s0090-4295(98)00641-4
  • Kuball J, Wen SF, Leissner J, et al. Successful adenovirus-mediated wild-type p53 gene transfer in patients with bladder cancer by intravesical vector instillation. J Clin Oncol. 2002;20(4):957–965. PubMed PMID: 11844817 DOI:10.1200/JCO.2002.20.4.957
  • Yamashita M, Rosser CJ, Zhou JH, et al. Syn3 provides high levels of intravesical adenoviral-mediated gene transfer for gene therapy of genetically altered urothelium and superficial bladder cancer. Cancer Gene Ther. 2002;9(8):687–691. PubMed PMID: 12136430 DOI:10.1038/sj.cgt.7700488
  • Connor RJ, Engler H, Machemer T, et al. Identification of polyamides that enhance adenovirus-mediated gene expression in the urothelium. Gene Ther. 2001;8(1):41–48. PubMed PMID: 11402300 DOI:10.1038/sj.gt.3301348
  • Benedict WF, Tao Z, Kim CS, et al. Intravesical Ad-IFNalpha causes marked regression of human bladder cancer growing orthotopically in nude mice and overcomes resistance to IFN-alpha protein. Mol Ther. 2004;10(3):525–532. PubMed PMID: 15336652 DOI:10.1016/j.ymthe.2004.05.027
  • Tao Z, Connor RJ, Ashoori F, et al. Efficacy of a single intravesical treatment with Ad-IFN/Syn 3 is dependent on dose and urine IFN concentration obtained: implications for clinical investigation. Cancer Gene Ther. 2006;13(2):125–130. PubMed PMID: 16082384 DOI:10.1038/sj.cgt.7700865
  • Iqbal Ahmed CM, Johnson DE, Demers GW, et al. Interferon alpha 2b gene delivery using adenoviral vector causes inhibition of tumor growth in xenograft models from a variety of cancers. Cancer Gene Ther. 2001;8(10):788–795. PubMed PMID: 11687902 DOI:10.1038/sj.cgt.7700364
  • Connor RJ, Anderson JM, Machemer T, et al. Sustained intravesical interferon protein exposure is achieved using an adenoviral-mediated gene delivery system: a study in rats evaluating dosing regimens. Urology. 2005;66(1):224–229. PubMed PMID: 15992886. DOI:10.1016/j.urology.2005.02.015
  • Nagabhushan TL, Maneval DC, Benedict WF, et al. Enhancement of intravesical delivery with Syn3 potentiates interferon-alpha2b gene therapy for superficial bladder cancer. Cytokine Growth Factor Rev. 2007;18(5–6):389–394. Epub 20070809 Epub 20070809 DOI:10.1016/j.cytogfr.2007.06.007
  • Li S, Rosenberg JE, Donjacour AA, et al. Rapid inhibition of cancer cell growth induced by lentiviral delivery and expression of mutant-template telomerase RNA and anti-telomerase short-interfering RNA. Cancer Res. 2004;64(14):4833–4840. PubMed PMID: 15256453 DOI:10.1158/0008-5472.CAN-04-0953
  • Kikuchi E, Menendez S, Ozu C, et al. Highly efficient gene delivery for bladder cancers by intravesically administered replication-competent retroviral vectors. Clin Cancer Res. 2007;13(15 Pt 1):4511–4518. PubMed PMID: 17671137 DOI:10.1158/1078-0432.CCR-07-0151
  • Siemens DR, Elzey BD, Lubaroff DM, et al. Cutting edge: restoration of the ability to generate CTL in mice immune to adenovirus by delivery of virus in a collagen-based matrix. J Immunol. 2001;166(2):731–735. PubMed PMID: 11145643 DOI:10.4049/jimmunol.166.2.731
  • Pagliaro LC, Keyhani A, Williams D, et al. Repeated intravesical instillations of an adenoviral vector in patients with locally advanced bladder cancer: a phase I study of p53 gene therapy. J Clin Oncol. 2003;21(12):2247–2253. PubMed PMID: 12805322 DOI:10.1200/JCO.2003.09.138
  • Mokkapati S, Narayan VM, Manyam GC, et al. Lentiviral interferon: a novel method for gene therapy in bladder cancer. Mol Ther Oncolytics. 2022;26:141–157. Epub 20220610 Epub 20220610. DOI:10.1016/j.omto.2022.06.005
  • Saoud R, Telfer S, Maruf M, et al. Mp16-14 Clinical outcomes of a randomized, prospective, phase II study to determine the efficacy of bacillus Calmette-Guerin (bcg) given in combination with panvac versus bcg given alone in adults with high grade bcg-refractory non-muscle invasive bladder cancer. J Urol. 2021;206(Supplement 3). DOI:10.1097/ju.0000000000002001.14
  • Smaldone MC, Davies BJ. BC-819, a plasmid comprising the H19 gene regulatory sequences and diphtheria toxin A, for the potential targeted therapy of cancers. Curr Opin Mol Ther. 2010;12(5): 607–616. PubMed PMID: 20886393.
  • Gofrit ON, Benjamin S, Halachmi S, et al. DNA based therapy with diphtheria toxin-A BC-819: a phase 2b marker lesion trial in patients with intermediate risk nonmuscle invasive bladder cancer. J Urol. 2014;191(6):1697–1702. Epub 20131214 Epub 20131214 DOI:10.1016/j.juro.2013.12.011
  • Li R, Steinberg GD, Uchio EM, et al. CORE1: phase 2, single-arm study of CG0070 combined with pembrolizumab in patients with nonmuscle-invasive bladder cancer (NMIBC) unresponsive to bacillus Calmette-Guerin (BCG). J Clin Oncol. 2022;40(16_suppl):4597.
  • Shore ND, Boorjian SA, Canter DJ, et al. 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. 2017;35(30):3410–3416. Epub 20170823 Epub 20170823 DOI:10.1200/JCO.2017.72.3064
  • Siefker-Radtke A, Zhang XQ, Guo CC, et al. A Phase l Study of a Tumor-targeted Systemic Nanodelivery System, SGT-94, in Genitourinary Cancers. Mol Ther. 2016;24(8):1484–1491. Epub 20160613 Epub 20160613 DOI:10.1038/mt.2016.118
  • Burke JM, Lamm DL, Meng MV, et al. A first in human phase 1 study of CG0070, a GM-CSF expressing oncolytic adenovirus, for the treatment of nonmuscle invasive bladder cancer. J Urol. 2012;188(6):2391–2397. Epub 20121022 Epub 20121022 DOI:10.1016/j.juro.2012.07.097
  • Portal DE, Weiss RE, Wojtowicz M, et al. Phase I neoadjuvant study of intravesical recombinant fowlpox-GM-CSF (Rf-GM-CSF) or fowlpox-TRICOM (Rf-TRICOM) in patients with bladder carcinoma. Cancer Gene Ther. 2020;27(6):438–447. Epub 20190620 Epub 20190620 DOI:10.1038/s41417-019-0112-z
  • Malmstrom PU, Loskog AS, Lindqvist CA, et al. AdCD40L immunogene therapy for bladder carcinoma–the first phase I/IIa trial. Clin Cancer Res. 2010;16(12):3279–3287. Epub 20100504 Epub 20100504 DOI:10.1158/1078-0432.CCR-10-0385
  • Packiam VT, Lamm DL, Barocas DA, et al. An open label, single-arm, phase II multicenter study of the safety and efficacy of CG0070 oncolytic vector regimen in patients with BCG-unresponsive non-muscle-invasive bladder cancer: interim results. Urol Oncol. 2018;36(10):440–447. Epub 20170726 Epub 20170726 DOI:10.1016/j.urolonc.2017.07.005
  • Halachmi S, Leibovitch I, Zisman A, et al. Phase II trial of BC-819 intravesical gene therapy in combination with BCG in patients with non-muscle invasive bladder cancer (NMIBC). J Clin Oncol. 2018;36(6_suppl):499.
  • Navai N, Benedict WF, Zhang G, et al. Phase 1b Trial to Evaluate Tissue Response to a Second Dose of Intravesical Recombinant Adenoviral Interferon alpha2b Formulated in Syn3 for Failures of Bacillus Calmette-Guerin (BCG) Therapy in Nonmuscle Invasive Bladder Cancer. Ann Surg Oncol. 2016;23(12):4110–4114. Epub 20160707 Epub 20160707 DOI:10.1245/s10434-016-5300-6
  • Dinney CP, Fisher MB, Navai N, et al. Phase I trial of intravesical recombinant adenovirus mediated interferon-alpha2b formulated in Syn3 for Bacillus Calmette-Guerin failures in nonmuscle invasive bladder cancer. J Urol. 2013;190(3):850–856. Epub 20130315 Epub 20130315 DOI:10.1016/j.juro.2013.03.030
  • Boorjian SA, Alemozaffar M, Konety BR, et al. Intravesical nadofaragene firadenovec gene therapy for BCG-unresponsive non-muscle-invasive bladder cancer: a single-arm, open-label, repeat-dose clinical trial. Lancet Oncol. 2021;22(1):107–117. Epub 20201127 Epub 20201127 DOI:10.1016/S1470-2045(20)30540-4
  • Bhindi B, Kool R, Kulkarni GS, et al. Canadian Urological Association guideline on the management of non-muscle-invasive bladder cancer - Abridged version. Can Urol Assoc J. 2021;15(8):230–239. PubMed PMID: 35099374; PubMed Central PMCID: PMC8418252 DOI:10.5489/cuaj.7487
  • Chang SS, Boorjian SA, Chou R, et al. Diagnosis and Treatment of Non-Muscle Invasive Bladder Cancer: aUA/SUO Guideline. J Urol. 2016;196(4):1021–1029.
  • Babjuk M, Burger M, Compérat E, et al. EAU Guidelines on Non-muscle-invasive Bladder Cancer (TaT1 and CIS). Edn presented at the 37th EAU Annual Congress, Amsterdam. 2022.
  • Steinberg G, Bahnson R, Brosman S, et al. Efficacy and safety of valrubicin for the treatment of Bacillus Calmette-Guerin refractory carcinoma in situ of the bladder The Valrubicin Study Group. J Urol. 2000;163(3):761–767. PubMed PMID: 10687972. DOI:10.1016/S0022-5347(05)67799-3
  • Balar AV, Kamat AM, Kulkarni GS, et al. Pembrolizumab monotherapy for the treatment of high-risk non-muscle-invasive bladder cancer unresponsive to BCG (KEYNOTE-057): an open-label, single-arm, multicentre, phase 2 study. Lancet Oncol. 2021;22(7):919–930. Epub 20210526 Epub 20210526 DOI:10.1016/S1470-2045(21)00147-9
  • Zhang Z, Shirakawa T, Hinata N, et al. Combination with CD/5-FC gene therapy enhances killing of human bladder-cancer cells by radiation. J Gene Med. 2003;5(10):860–867. PubMed PMID: 14533194 DOI:10.1002/jgm.408
  • Matsumoto K, Freund CT, Teh BS, et al. Novel therapeutic approach for bladder cancer: synergistic effects with combined radiation and suicide gene therapy using a chimeric adenovirus vector. Int J Radiat Oncol Biol Phys. 2004;60(1):S376–7. DOI:10.1016/j.ijrobp.2004.07.232

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