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Review

Recombinant bacillus Calmette-Guérin in urothelial bladder cancer immunotherapy: current strategies

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References

  • Morales A, Eidinger D, Bruce AW. Intracavitary Bacillus Calmette-Guerin in the treatment of superficial bladder tumors. J Urol 1976;116(2):180-3
  • Herr HW, Morales A. History of bacillus Calmette-Guerin and bladder cancer: an immunotherapy success story. J Urol 2008;179(1):53-6
  • Gontero P, Bohle A, Malmstrom PU, et al. The role of Bacillus Calmette-Guérin in the treatment of non–muscle-invasive bladder cancer. Eur Urol 2010;57(3):410-29
  • Madbouly K. Intravesical bacillus Calmette-Guerin for bladder cancer: what is known? What is not? What is next? Urol Ann 2013;5(2):108-9
  • Brausi M, Oddens J, Sylvester R, et al. Side effects of Bacillus Calmette-Guérin (BCG) in the treatment of intermediate- and high-risk Ta, T1 papillary carcinoma of the bladder: results of the EORTC genito-urinary cancers group randomised phase 3 study comparing one-third dose with full dose and 1 year with 3 years of maintenance BCG. Eur Urol 2014;65(1):69-76
  • Alexandroff AB, Nicholson S, Patel PM, et al. Recent advances in bacillus Calmette-Guerin immunotherapy in bladder cancer. Immunotherapy 2010;2(4):551-60
  • Askeland EJ, Newton MR, O’Donnell MA, et al. Bladder Cancer Immunotherapy: BCG and Beyond. Adv Urol 2012;2012:181987
  • Kawai K, Miyazaki J, Joraku A, et al. Bacillus Calmette-Guerin (BCG) immunotherapy for bladder cancer: current understanding and perspectives on engineered BCG vaccine. Cancer Sci 2013;104(1):22-7
  • Siegel R, Ma J, Zou Z, Jemal A. Cancer Statistics, 2014. CA Cancer J Clin 2014;64(1):9-29
  • Babjuk M, Burger M, Zigeuner R, et al. EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: update 2013. Eur Urol 2013;64(4):639-53
  • Shelley MD, Kynaston H, Court J, et al. A systematic review of intravesical bacillus Calmette-Guérin plus transurethral resection vs transurethral resection alone in Ta and T1 bladder cancer. BJU Int 2001;88(3):209-16
  • Böhle A, Jocham D, Bock PR. Intravesical bacillus Calmette-Guerin versus mitomycin C for superficial bladder cancer: a formal metaanalysis of comparative studies on recurrence and toxicity. J Urol 2003;169(1):90-5
  • Shelley MD, Wilt TJ, Court J, et al. Intravesical bacillus Calmette-Guérin is superior to mitomycin C in reducing tumour recurrence in high-risk superficial bladder cancer: a metaanalysis of randomized trials. BJU Int 2004;93(4):485-90
  • Han RF, Pan JG. Can intravesical bacillus Calmette-Guérin reduce recurrence in patients with superficial bladder cancer? A metaanalysis of randomized trials. Urology 2006;67(6):1216-23
  • Malmström PU, Sylvester RJ, Crawford DE, et al. An individual patient data meta-analysis of the long-term outcome of randomised studies comparing intravesical mitomycin C versus bacillus Calmette-Guérin for non-muscle-invasive bladder cancer. Eur Urol 2009;56(2):247-56
  • Brandau S, Suttmann H. Thirty years of BCG immunotherapy for non-muscle invasive bladder cancer: a success story with room for improvement. Biomed Pharmacother 2007;61(6):299-305
  • Redelman-Sidi G, Glickman MS, Bochner BH. The mechanism of action of BCG therapy for bladder cancer--a current perspective. Nat Rev Urol 2014;11(3):153-62
  • Becich MJ, Carroll S, Ratliff TL. Internalization of bacilli Calmette-Guerin by bladder tumor cells. J Urol 1991;145(6):1316-24
  • de Reijke TM, de Boer EC, Kurth KH, et al. Urinary cytokines during intravesicalbacillus Calmette-Guerin therapy for superficial bladder cancer: processing, stability and prognostic value. J Urol 1996;155(2):477-82
  • Luo Y, Chen X, O’Donnell MA. Role of Th1 and Th2 cytokines in BCG-induced IFN-γ production: cytokine promotion and simulation of BCG effect. Cytokine 2003;21(1):17-26
  • Sapre N, Corcoran NM. Modulating the immune response to Bacillus Calmette-Guérin (BCG): a novel way to increase the immunotherapeutic effect of BCG for treatment of bladder cancer? BJU Int 2013;112(6):852-3
  • Zlotta AR, Fleshner NE, Jewett MA. The management of BCG failure in non-muscle-invasive bladder cancer: an update. Can Urol Assoc 2009;3(6 Suppl 4):S199-205
  • Ohara N, Yamada T. Recombinant BCG vaccines. Vaccine 2001;19(30):4089-98
  • Luo Y, Henning J, O’Donnell MA. Th1 cytokine-secreting recombinant Mycobacterium bovis bacillus Calmette-Guérin and prospective use in immunotherapy of bladder cancer. Clin Dev Immunol 2011;2011:728930
  • Lotze MT, Grimm EA, Mazumder A, et al. Lysis of fresh and cultured autologous tumor by human lymphocytes cultured in T-cell growth factor. Cancer Res 1981;41(11 Pt 1):4420-5
  • Henney CS, Kuribayashi K, Kern DE, et al. Interleukin-2 augments natural killer cell activity. Nature 1981;291(5813):335-8
  • Malkovský M, Loveland B, North M, et al. Recombinant interleukin-2 directly augments the cytotoxicity of human monocytes. Nature 1987;325(6101):262-5
  • Ratliff TL, Haaff EO, Catalona WJ. Interleukin-2 production during intravesical bacille Calmette-Guerin therapy for bladder cancer. Clin Immunol Immunopathol 1986;40(2):375-9
  • De Jong WH, De Boer EC, Van der Meijden AP, et al. Presence of interleukin-2 in urine of superficial bladder cancer patients after intravesical treatment with bacillus Calmette-Guérin. Cancer Immunol Immunother 1990;31(3):182-6
  • de Reijke TM, De Boer EC, Kurth KH, et al. Urinary interleukin-2 monitoring during prolonged bacillus Calmette-Guerin treatment: can it predict the optimal number of instillations? J Urol 1999;161(1):67-71
  • Saint F, Patard JJ, Maille P, et al. Prognostic value of a T helper 1 urinary cytokine response after intravesical bacillus Calmette-Guerin treatment for superficial bladder cancer. J Urol 2002;167(1):364-7
  • O’Donnell MA, Aldovini A, Duda RB, et al. Recombinant Mycobacterium bovis BCG secreting functional interleukin-2 enhances gamma interferon production by splenocytes. Infect Immun 1994;62(6):2508-14
  • Murray PJ, Aldovini A, Young RA. Manipulation and potentiation of antimycobacterial immunity using recombinant bacille Calmette-Guérin strains that secrete cytokines. Proc Natl Acad Sci USA 1996;93(2):934-9
  • Slobbe L, Lockhart E, O’Donnell MA, et al. An in vivo comparison of bacillus Calmette-Guérin (BCG) and cytokine-secreting BCG vaccines. Immunology 1999;96(4):517-23
  • Luo Y, Chen X, Szilvasi A, et al. Co-expression of interleukin-2 and green fluorescent protein reporter in mycobacteria: in vivo application for monitoring antimycobacterial immunity. Mol Immunol 2000;37(9):527-36
  • Young S, O’Donnell M, Lockhart E, et al. Manipulation of immune responses to Mycobacterium bovis by vaccination with IL-2- and IL-18-secreting recombinant bacillus Calmette Guerin. Immunol Cell Biol 2002;80(3):209-15
  • Fan XL, Yu TH, Gao Q, et al. Immunological properties of recombinant Mycobacterium bovis bacillus Calmette-Guérin strain expressing fusion protein IL-2-ESAT-6. Acta Biochim Biophys Sin (Shanghai) 2006;38(10):683-90
  • Chen X, O’Donnell MA, Luo Y. Dose-dependent synergy of Th1-stimulating cytokines on bacille Calmette-Guérin-induced interferon-gamma production by human mononuclear cells. Clin Exp Immunol 2007;149(1):178-85
  • Yamada H, Matsumoto S, Matsumoto T, et al. Murine IL-2 secreting recombinant Bacillus Calmette-Guerin augments macrophage-mediated cytotoxicity against murine bladder cancer MBT-2. J Urol 2000;164(2):526-31
  • Luo Y, Yamada H, Evanoff DP, et al. Role of Th1-stimulating cytokines in bacillus Calmette-Guérin (BCG)-induced macrophage cytotoxicity against mouse bladder cancer MBT-2 cells. Clin Exp Immunol 2006;146(1):181-8
  • Brunda MJ, Luistro L, Warrier RR, et al. Antitumor and antimetastatic activity of interleukin 12 against murine tumors. J Exp Med 1993;178(4):1223-30
  • Nastala CL, Edington HD, McKinney TG, et al. Recombinant IL-12 administration induces tumor regression in association with IFN-gamma production. J Immunol 1994;153(4):1697-706
  • Coughlin CM, Salhany KE, Wysocka M, et al. Interleukin-12 and interleukin-18 synergistically induce murine tumor regression which involves inhibition of angiogenesis. J Clin Invest 1998;101(6):1441-52
  • Kawamura T, Takeda K, Mendiratta SK, et al. Cutting edge: critical role of NK1 T cells in IL-12-induced immune responses in vivo. J Immunol 1998;160(1):16-19
  • O’Donnell MA, Luo Y, Hunter SE, et al. Interleukin-12 immunotherapy of murine transitional cell carcinoma of the bladder: dose dependent tumor eradication and generation of protective immunity. J Urol 2004;171(3):1330-5
  • Horinaga M, Harsch KM, Fukuyama R, et al. Intravesical interleukin-12 gene therapy in an orthotopic bladder cancer model. Urology 2005;66(2):461-6
  • Zaharoff DA, Hoffman BS, Hooper HB, et al. Intravesical immunotherapy of superficial bladder cancer with chitosan/interleukin-12. Cancer Res 2009;69(15):6192-9
  • Weiss GR, O’Donnell MA, Loughlin K, et al. Phase 1 study of the intravesical administration of recombinant human interleukin-12 in patients with recurrent superficial transitional cell carcinoma of the bladder. J Immunother 2003;26(4):343-8
  • Hao M, Bao L, GAO L, Zhang HD. Construction and screen of recombinant BCG strain expressing and secreting human interleukin 12 protein. Sichuan Da Xue Xue Bao Yi Xue Ban 2007;38(2):186-9
  • Deng Y, Bao L, Yang X. Evaluation of immunogenicity and protective efficacy against Mycobacterium tuberculosis infection elicited by recombinant Mycobacterium bovis BCG expressing human Interleukin-12p70 and Early Secretory Antigen Target-6 fusion protein. Microbiol Immunol 2011;55(11):798-808
  • Lin CW, Su IJ, Chang JR, et al. Recombinant BCG coexpressing Ag85B, CFP10, and interleukin-12 induces multifunctional Th1 and memory T cells in mice. APMIS 2012;120(1):72-82
  • Xu D, Chan WL, Leung BP, et al. Selective expression and functions of interleukin 18 receptor on T helper (Th) type 1 but not Th2 cells. J Exp Med 1998;188(8):1485-92
  • Kohno K, Kataoka J, Ohtsuki T, et al. IFN-gamma-inducing factor (IGIF) is a costimulatory factor on the activation of Th1 but not Th2 cells and exerts its effect independently of IL-12. J Immunol 1997;158(4):1541-50
  • Ahn HJ, Maruo S, Tomura M, et al. A mechanism underlying synergy between IL-12 and IFN-gamma-inducing factor in enhanced production of IFN-gamma. J Immunol 1997;159(5):2125-31
  • Luo Y, Chen X, O’Donnell MA. Role of Th1 and Th2 cytokines in BCG-induced IFN-gamma production: cytokine promotion and simulation of BCG effect. Cytokine 2003;21(1):17-26
  • Thalmann GN, Sermier A, Rentsch C, et al. Urinary Interleukin-8 and 18 predict the response of superficial bladder cancer to intravesical therapy with bacillus Calmette-Guérin. J Urol 2000;164(6):2129-33
  • Luo Y, Yamada H, Chen X, et al. Recombinant Mycobacterium bovis bacillus Calmette-Guérin (BCG) expressing mouse IL-18 augments Th1 immunity and macrophage cytotoxicity. Clin Exp Immunol 2004;137(1):24-34
  • Jonasch E, Haluska FG. Interferon in oncological practice: review of interferon biology, clinical applications, and toxicities. Oncologist 2001;6(1):34-55
  • Papageorgiou A, Dinney CP, McConkey DJ. Interferon-α induces TRAIL expression and cell death via an IRF-1-dependentmechanism in human bladder cancer cells. Cancer Biol Ther 2007;6(6):872-9
  • Slaton JW, Perrotte P, Inoue K, et al. Interferon-α-mediated down-regulation of angiogenesis-related genes and therapy of bladder cancer are dependent on optimization of biological dose and schedule. Clin Cancer Res 1999;5(10):2726-34
  • O’Donnell MA, Krohn J, DeWolf WC. Salvage intravesical therapy with interferon-α2B plus low dose bacillus Calmette-Guérin is effective in patients with superficial bladder cancer in whom bacillus Calmette-Guerin alone previously failed. J Urol 2001;166(4):1300-4
  • Lam JS, Benson MC, O’Donnell MA, et al. Bacillus Calmette-Guérin plus interferon-α2B intravesical therapy maintains an extended treatment plan for superficial bladder cancer with minimal toxicity. Urol Oncol 2003;21(5):354-60
  • Joudi FN, Smith BJ, O’Donnell MA, et al. Final results from a national multicenter phase II trial of combination bacillus Calmette-Guérin plus interferon α-2B for reducing recurrence of superficial bladder cancer. Urol Oncol 2006;24(4):344-8
  • Bazarbashi S, Soudy H, Abdelsalam M, et al. Coadministration of intravesical bacillus Calmette-Guérin and interferon α-2B as first line in treating superficial transitional cell carcinoma of the urinary bladder. BJU Int 2011;108(7):1115-18
  • Luo Y, Chen X, Han R, et al. Recombinant bacillus Calmette-Guérin (BCG) expressing human interferon-alpha 2B demonstrates enhanced immunogenicity. Clin Exp Immunol 2001;123(2):264-70
  • Liu W, O’Donnell MA, Chen X, et al. Recombinant bacillus Calmette-Guérin (BCG) expressing interferon-alpha 2B enhances human mononuclear cell cytotoxicity against bladder cancer cell lines in vitro. Cancer Immunol Immunother 2009;58(10):1647-55
  • Ding GQ, Yu YL, Shen ZJ, et al. Antitumor effects of human interferon-alpha 2b secreted by recombinant bacillus Calmette-Guérin vaccine on bladder cancer cells. J Zhejiang Univ Sci B 2012;13(5):335-41
  • Hawkyard SJ, Jackson AM, James K, et al. The inhibitory effects of interferon gamma on the growth of bladder cancer cells. J Urol 1992;147(5):1399-403
  • Hawkyard SJ, Jackson AM, Prescott S, et al. The effect of recombinant cytokines on bladder cancer cells in vitro. J Urol 1993;150(2 Pt 1):514-18
  • O’Donnell MA, Luo Y, Chen X, et al. Role of IL-12 in the induction and potentiation of IFN-gamma in response to bacillus Calmette-Guérin. J Immunol 1999;163(8):4246-52
  • Riemensberger J, Böhle A, Brandau S. IFN-gamma and IL-12 but not IL-10 are required for local tumour surveillance in a syngeneic model of orthotopic bladder cancer. Clin Exp Immunol 2002;127(1):20-6
  • Arnold J, de Boer EC, O’Donnell MA, et al. Immunotherapy of experimental bladder cancer with recombinant BCG expressing interferon-gamma. J Immunother 2004;27(2):116-23
  • Stein P. E, Boodhoo A, Armstrong GD, et al. The crystal structure of pertussis toxin. Structure 1994;2(1):45-57
  • Nascimento IP, Dias WO, Mazzantini RP, et al. Recombinant Mycobacterium bovis BCG expressing pertussis toxin subunit S1 induces protection against an intracerebral challenge with live Bordetella pertussis in mice. Infect Immun 2000;68(9):4877-83
  • Chade DC, Borra RC, Nascimento IP, et al. Immunomodulatory effects of recombinant BCG expressing pertussis toxin on TNF-alpha and IL-10 in a bladder cancer model. J Exp Clin Cancer Res 2008;27(1):78
  • Andrade PM, Chade DC, Borra RC, et al. The therapeutic potential of recombinant BCG expressing the antigen S1PT in the intravesical treatment of bladder cancer. Urol Oncol 2010;28(5):520-5
  • Zlotta AR, Van Vooren JP, Denis O, et al. What are the immunologically active components of bacille Calmette-Guérin in therapy of superficial bladder cancer? Int J Cancer 2000;87(6):844-52
  • Chin JL, Kadhim SA, Batislam E, et al. Mycobacterium cell wall: an alternative to intravesical bacillus Calmette-Guerin (BCG) therapy in orthotopic murine bladder cancer. J Urol 1996;156(3):1189-93
  • Morales A, Chin JL, Ramsey EW. Mycobacterial cell wall extract for treatment of carcinoma in situ of the bladder. J Urol 2001;166(5):1633-7
  • Morales A, Phadke K, Steinhoff G. Intravesical mycobacterial cell wall-DNA complex in the treatment of carcinoma in situ of the bladder after standard intravesical therapy has failed. J Urol 2009;181(3):1040-5
  • Mycobacterial Cell Wall-DNA Complex in Treatment of BCG-refractory Patients With Non-muscle Invasive Bladder Cancer. Available from: www.clinicaltrials.gov/ct2/results?term=NCT00406068&Search=Search
  • Efficacy and Safety Evaluation of EN3348 (Mycobacterial Cell Wall-DNA Complex [MCC]) as Compared With Mitomycin C in the Intravesical Treatment of Subjects With BCG Recurrent/Refractory Non-muscle Invasive Bladder Cancer. Available from: www.clinicaltrials.gov/ct2/results?term=NCT01200992&Search=Search
  • Kato T, Bilim V, Yuuki K, et al. Bacillus Calmette-Guerin and BCG cell wall skeleton suppressed viability of bladder cancer cells in vitro. Anticancer Res 2010;30(10):4089-96
  • Joraku A, Homhuan A, Kawai K, et al. Immunoprotection against murine bladder carcinoma by octaarginine-modified liposomes incorporating cell wall of Mycobacterium bovis Bacillus Calmette-Guerin. BJU Int 2009;103(5):686-93
  • Miyazaki J, Nishiyama H, Yano I, et al. The therapeutic effects of R8-liposome-BCG-CWS on BBN-induced rat urinary bladder carcinoma. Anticancer Res 2011;31(6):2065-71
  • Nakamura T, Fukiage M, Higuchi M, et al. Nanoparticulation of BCG-CWS for application to bladder cancer therapy. J Control Release 2014;176:44-53
  • Begnini KR, Rizzi C, Campos VF, et al. Auxotrophic recombinant Mycobacterium bovis BCG overexpressing Ag85B enhances cytotoxicity on superficial bladder cancer cells in vitro. Appl Microbiol Biotechnol 2013;97(4):1543-52
  • Yu DS, Lee CF, Chang SY. Immunotherapy for orthotopic murine bladder cancer using bacillus Calmette-Guerin recombinant protein Mpt-64. J Urol 2007;177(2):738-42
  • Sänger C, Busche A, Bentien G, et al. Immunodominant PstS1 antigen of mycobacterium tuberculosis is a potent biological response modifier for the treatment of bladder cancer. BMC Cancer 2004;4:86
  • Yu DS, Lee CF, Hsieh DS, et al. Antitumor effects of recombinant BCG and interleukin-12 DNA vaccines on xenografted murine bladder cancer. Urology 2004;63(3):596-601
  • Lee CF, Chang SY, Hsieh DS, et al. Treatment of bladder carcinomas using recombinant BCG DNA vaccines and electroporative gene immunotherapy. Cancer Gene Ther 2004;11(3):194-207
  • Lee CF, Chang SY, Hsieh DS, et al. Immunotherapy for bladder cancer using recombinant bacillus Calmette-Guerin DNA vaccines and interleukin-12 DNA vaccine. J Urol 2004;171(3):1343-7
  • Saint F, Salomon L, Quintela R, et al. Do prognostic parameters of remission versus relapse after bacillus Calmette-Guerin (BCG) immunotherapy exist? Analysis of a quarter century of literature. Eur Urol 2003;43(4):351-60. discussion 360-361
  • Basturk B, Yavascaoglu I, Oral B, et al. Cytokine gene polymorphisms can alter the effect of bacillus Calmette-Guerin (BCG) immunotherapy. Cytokine 2006;35(1-2):1-5
  • Ahirwar D, Kesarwani P, Manchanda PK, et al. Anti- and proinflammatory cytokine gene polymorphism and genetic predisposition: association with smoking, tumor stage and grade, and bacillus Calmette-Guerin immunotherapy in bladder cancer. Cancer Genet Cytogenet 2008;184(1):1-8
  • Yuan S, Shi C, Han W, et al. Effective anti-tumor responses induced by recombinant bacillus Calmette-Guerin vaccines based on different tandem repeats of MUC1 and GM-CSF. Eur J Cancer Prev 2009;18(5):416-23
  • Yuan S, Shi C, Lv Y, et al. A novel Bacillus Calmette-Guerin-based breast cancer vaccine that coexpresses multiple tandem repeats of MUC1 and CD80 breaks the immune tolerance and inhibits MUC1-positive breast cancer growth. Cancer Biother Radiopharm 2009;24(5):607-13
  • Inman BA, Sebo TJ, Frigola X, et al. PD-L1 (B7-H1) expression by urothelial carcinoma of the bladder and BCG-induced granulomata: associations with localized stage progression. Cancer 2007;109(8):1499-505
  • Wang Y, Zhuang Q, Zhou S, et al. Costimulatory molecule B7-H1 on the immune escape of bladder cancer and its clinical significance. J Huazhong Univ Sci Technolog Med Sci 2009;29(1):77-9

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