Mycobacterium bovis bacillus Calmette-Guérin-induced macrophage cytotoxicity against bladder cancer cells

Yi Luo, Matthew J Knudson, Yi Luo, Matthew J Knudson

Abstract

Many details of the molecular and cellular mechanisms involved in Mycobacterium bovis bacillus Calmette-Guérin (BCG) immunotherapy of bladder cancer have been discovered in the past decades. However, information on a potential role for macrophage cytotoxicity as an effector mechanism is limited. Macrophages play pivotal roles in the host innate immunity and serve as a first line of defense in mycobacterial infection. In addition to their function as professional antigen-presenting cells, the tumoricidal activity of macrophages has also been studied with considerable interest. Studies have shown that activated macrophages are potent in killing malignant cells of various tissue origins. This review summarizes the current understanding of the BCG-induced macrophage cytotoxicity toward bladder cancer cells with an intention to inspire investigation on this important but underdeveloped research field.

References

    1. Morales A, Eidinger D, Bruce AW. Intracavitary Bacillus Calmette Guerin in the treatment of superficial bladder tumors. Journal of Urology. 1976;116(2):180–183.
    1. Alexandroff AB, Jackson AM, O’Donnell MA, James K. BCG immunotherapy of bladder cancer: 20 years on. Lancet. 1999;353(9165):1689–1694.
    1. Patard JJ, Saint F, Velotti F, Abbou CC, Chopin DK. Immune response following intravesical bacillus Calmette-Guerin instillations in superficial madder cancer: a review. Urological Research. 1998;26(3):155–159.
    1. Ratliff TL, Ritchey JK, Yuan JJJ, Andriole GL, Catalona WJ. T-cell subsets required for intravesical BCG immunotherapy for bladder cancer. Journal of Urology. 1993;150(3):1018–1023.
    1. Wang R, Rogers AM, Ratliff TL, Russell JH. CD95-dependent bystander lysis caused by CD4+ T helper 1 effectors. Journal of Immunology. 1996;157(7):2961–2968.
    1. Brandau S, Riemensberger J, Jacobsen M, et al. NK cells are essential for effective BCG immunotherapy. International Journal of Cancer. 2001;92(5):697–702.
    1. Liu W, O’Donnell MA, Chen X, Han R, Luo Y. Recombinant bacillus Calmette-Guérin (BCG) expressing interferon-alpha 2B enhances human mononuclear cell cytotoxicity against bladder cancer cell lines in vitro. Cancer Immunology, Immunotherapy. 2009;58(10):1647–1655.
    1. Wang M-H, Flad H-D, Böhle A, Chen Y-Q, Ulmer AJ. Cellular cytotoxicity of human natural killer cells and lymphokine-activated killer cells against bladder carcinoma cell lines. Immunology Letters. 1991;27(3):191–198.
    1. Shemtov MM, Cheng DL-W, Kong L, et al. LAK cell mediated apoptosis of human bladder cancer cells involves a pH-dependent endonuclease system in the cancer cell: possible mechanism of BCG therapy. Journal of Urology. 1995;154(1):269–274.
    1. Thanhäuser A, Böhle A, Flad H-D, Ernst M, Mattern T, Ulmer AJ. Induction of bacillus-Calmette-Guerin-activated killer cells from human peripheral blood mononuclear cells against human bladder carcinoma cell lines in vitro. Cancer Immunology Immunotherapy. 1993;37(2):105–111.
    1. Brandau S, Suttmann H, Riemensberger J, et al. Perforin-mediated lysis of tumor cells by Mycobacterium Bovis Bacillus Calmette-Guerin-activated killer cells. Clinical Cancer Research. 2000;6(9):3729–3738.
    1. Böhle A, Thanhäuser A, Ulmer AJ, Ernst M, Flad H-D, Jocham D. Dissecting the immunobiological effects of Bacillus Calmette-Guerin (BCG) in vitro: evidence of a distinct BCG-activated killer (BAK) cell phenomenon. Journal of Urology. 1993;150(6):1932–1937.
    1. Kawashima T, Norose Y, Watanabe Y, et al. Cutting edge: major CD8 T cell response to live bacillus Calmette-Guérin is mediated by CD1 molecules. Journal of Immunology. 2003;170(11):5345–5348.
    1. Wang M-H, Chen Y-Q, Gercken J, et al. Specific activation of human peripheral blood γ/δ+ T lymphocytes by sonicated antigens of Mycobacterium tuberculosis: role in vitro in killing human bladder carcinoma cell lines. Scandinavian Journal of Immunology. 1993;38(3):239–246.
    1. Higuchi T, Shimizu M, Owaki A, et al. A possible mechanism of intravesical BCG therapy for human bladder carcinoma: involvement of innate effector cells for the inhibition of tumor growth. Cancer Immunology, Immunotherapy. 2009;58(8):1245–1255.
    1. Naoe M, Ogawa Y, Takeshita K, et al. Bacillus Calmette-Guérin-pulsed dendritic cells stimulate natural killer T cells and γ δT cells. International Journal of Urology. 2007;14(6):532–538.
    1. Emoto M, Emoto Y, Buchwalow IB, Kaufmann SHE. Induction of IFN-γ-producing CD4+ natural killer T cells by Mycobacterium bovis bacillus Calmette Guerin. European Journal of Immunology. 1999;29(2):650–659.
    1. Suttmann H, Riemensberger J, Bentien G, et al. Neutrophil granulocytes are required for effective Bacillus Calmette-Guérin immunotherapy of bladder cancer and orchestrate local immune responses. Cancer Research. 2006;66(16):8250–8257.
    1. Rosevear HM, Lightfoot AJ, O'Donnell MA, Griffith TS. The role of neutrophils and TNF-related apoptosis-inducing ligand (TRAIL) in bacillus Calmette-Guérin (BCG) immunotherapy for urothelial carcinoma of the bladder. Cancer Metastasis Reviews. 2009;28(3-4):345–353.
    1. Klostergaard J, Stoltje PA, Kull FC., Jr. Tumoricidal effector mechanisms of murine BCG-activated macrophages: role of TNF in conjugation-dependent and conjugation-independent pathways. Journal of Leukocyte Biology. 1990;48(3):220–228.
    1. Klostergaard J, Leroux ME, Hung M-C. Cellular models of macrophage tumoricidal effector mechanisms in vitro. Characterization of cytolytic responses to tumor necrosis factor and nitric oxide pathways in vitro. Journal of Immunology. 1991;147(8):2802–2808.
    1. Schwamberger G, Flesch I, Ferber E. Tumoricidal effector molecules of murine macrophages. Pathobiology. 1991;59(4):248–253.
    1. Böhle A, Gerdes J, Ulmer AJ, Hofstetter AG, Flad H-D. Effects of local bacillus Calmette-Guerin therapy in patients with bladder carcinoma on immunocompetent cells of the bladder wall. Journal of Urology. 1990;144(1):53–58.
    1. Prescott S, James K, Hargreave TB, Chisholm GD, Smyth JF. Intravesical Evans strain BCG therapy: quantitative immunohistochemical analysis of the immune response within the bladder wall. Journal of Urology. 1992;147(6):1636–1642.
    1. Peuchmaur M, Benoit G, Vieillefond A, et al. Analysis of mucosal bladder leucocyte subpopulations in patients treated with intravesical bacillus calmette-guerin. Urological Research. 1989;17(5):299–303.
    1. Saint F, Patard JJ, Groux Muscatelli B, et al. Evaluation of cellular tumour rejection mechanisms in the peritumoral bladder wall after bacillus Calmette-Guérin treatment. British Journal of Urology International. 2001;88(6):602–610.
    1. De Boer EC, De Jong WH, Van der Meijden APM, et al. Leukocytes in the urine after intravesical BCG treatment for superficial bladder cancer. A flow cytofluorometric analysis. Urological Research. 1991;19(1):45–50.
    1. De Boer EC, De Jong WH, Van der Meijden APM, et al. Presence of activated lymphocytes in the urine of patients with superficial bladder cancer after intravesical immunotherapy with bacillus Calmette-Guerin. Cancer Immunology Immunotherapy. 1991;33(6):411–416.
    1. De Boer EC, De Jong WH, Steerenberg PA, et al. Leukocytes and cytokines in the urine of superficial bladder cancer patients after intravesical immunotherapy with Bacillus Calmette-Guerine. In Vivo. 1991;5(6):671–678.
    1. Böhle A, Nowc NCH, Ulmer AJ, et al. Elevations of cytokines interleukin-1, interleukin-2 and tumor necrosis factor in the urine of patients after intravesical bacillus Calmette-Guerin immunotherapy. Journal of Urology. 1990;144(1):59–64.
    1. Thalmann GN, Sermier A, Rentsch C, Möhrle K, Cecchini MG, Studer UE. Urinary interleukin-8 and 18 predict the response of superficial bladder cancer to intravesical therapy with bacillus Calmette-Guerin. Journal of Urology. 2000;164(6):2129–2133.
    1. De Reijke TM, De Boer EC, Kurth KH, Schamhart DHJ. Urinary cytokines during intravesical bacillus Calmette-Guerin therapy for superficial bladder cancer: processing, stability and prognostic value. Journal of Urology. 1996;155(2):477–482.
    1. 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. Journal of Urology. 2002;167(1):364–367.
    1. Nadler R, Luo Y, Zhao W, et al. Interleukin 10 induced augmentation of delayed-type hypersensitivity (DTH) enhances Mycobacterium bovis bacillus Calmette-Guérin (BCG) mediated antitumour activity. Clinical and Experimental Immunology. 2003;131(2):206–216.
    1. Luo Y, Chen X, O’Donnell MA. Mycobacterium bovis bacillus Calmette-Guérin (BCG) induces human CC- and CXC-chemokines in vitro and in vivo. Clinical and Experimental Immunology. 2007;147(2):370–378.
    1. Wang J, Wakeham J, Harkness R, Xing Z. Macrophages are a significant source of type 1 cytokines during mycobacterial infection. Journal of Clinical Investigation. 1999;103(7):1023–1029.
    1. Atkinson S, Valadas E, Smith SM, Lukey PT, Dockrell HM. Monocyte-derived macrophage cytokine responses induced by M. bovis BCG. Tubercle and Lung Disease. 2000;80(4-5):197–207.
    1. Calorini L, Bianchini F, Mannini A, et al. IFNγ and TNFα account for a pro-clonogenic activity secreted by activated murine peritoneal macrophages. Clinical and Experimental Metastasis. 2002;19(3):259–264.
    1. Baran J, Baj-Krzyworzeka M, Weglarczyk K, Ruggiero I, Zembala M. Modulation of monocyte-tumour cell interactions by Mycobacterium vaccae . Cancer Immunology, Immunotherapy. 2004;53(12):1127–1134.
    1. Pryor K, Goddard J, Goldstein D, et al. Bacillus Calmette-Guerin (BCG) enhances monocyte- and lymphocyte-mediated bladder tumour cell killing. British Journal of Cancer. 1995;71(4):801–807.
    1. Yamada H, Matsumoto S, Matsumoto T, Yamada T, Yamashita U. Murine IL-2 secreting recombinant Bacillus Calmette-Guerin augments macrophage-mediated cytotoxicity against murine bladder cancer MBT-2. Journal of Urology. 2000;164(2):526–531.
    1. Yamada H, Matsumoto S, Matsumoto T, Yamada T, Yamashita U. Enhancing effect of an inhibitor of nitric oxide synthesis on Bacillus Calmette-Guerin-induced macrophage cytotoxicity against murine bladder cancer cell line MBT-2 in vitro. Japanese Journal of Cancer Research. 2000;91(5):534–542.
    1. Yamada H, Kuroda E, Matsumoto S, Matsumoto T, Yamada T, Yamashita U. Prostaglandin E2 down-regulates viable Bacille Calmette-Guérin-induced macrophage cytotoxicity against murine bladder cancer cell MBT-2 in vitro. Clinical and Experimental Immunology. 2002;128(1):52–58.
    1. Luo Y, Yamada H, Chen X, et al. Recombinant Mycobacterium bovis bacillus Calmette-Guérin (BCG) expressing mouse IL-18 augmente Th1 immunity and macrophage cytotoxicity. Clinical and Experimental Immunology. 2004;137(1):24–34.
    1. Luo Y, Yamada H, Evanoff DP, Chen X. Role of Th1-stimulating cytokines in bacillus Calmette-Guérin (BCG)-induced macrophage cytotoxicity against mouse bladder cancer MBT-2 cells. Clinical and Experimental Immunology. 2006;146(1):181–188.
    1. Luo Y, Han R, Evanoff DP, Chen X. Interleukin-10 inhibits Mycobacterium bovis bacillus Calmette-Guérin (BCG)-induced macrophage cytotoxicity against bladder cancer cells. Clinical and Experimental Immunology. 2010;160(3):359–368.
    1. Ratliff TL. Bacillus Calmette-Guerin (BCG): mechanism of action in superficial bladder cancer. Urology. 1991;37(5, supplement):8–11.
    1. Bevers RFM, Kurth K-H, Schamhart DHJ. Role of urothelial cells in BCG immunotherapy for superficial bladder cancer. British Journal of Cancer. 2004;91(4):607–612.
    1. Smith WL, Garavito RM, DeWitt DL. Prostaglandin endoperoxide H syntheses (cyclooxygenases)-1 and -2. Journal of Biological Chemistry. 1996;271(52):33157–33160.
    1. Arnold J, De Boer EC, O’Donnell MA, Böhle A, Brandau S. Immunotherapy of experimental bladder cancer with recombinant BCG expressing interferon-γ . Journal of Immunotherapy. 2004;27(2):116–123.
    1. Horinaga M, Harsch KM, Fukuyama R, Heston W, Larchian W. Intravesical interleukin-12 gene therapy in an orthotopic bladder cancer model. Urology. 2005;66(2):461–466.
    1. DesJardin LE, Kaufman TM, Potts B, Kutzbach B, Yi H, Schlesinger LS. Mycobacterium tuberculosis-infected human macrophages exhibit enhanced cellular adhesion with increased expression of LFA-1 and ICAM-1 and reduced expression and/or function of complement receptors, FcγRII and the mannose receptor. Microbiology. 2002;148(10):3161–3171.
    1. Mustafa T, Phyu S, Nilsen R, Bjune G, Jonsson R. Increased expression of Fas ligand on Mycobacterium tuberculosis infected macrophages: a potential novel mechanism of immune evasion by Mycobacterium tuberculosis? Inflammation. 1999;23(6):507–521.
    1. Diehl GE, Yue HH, Hsieh K, et al. TRAIL-R as a negative regulator of innate immune cell responses. Immunity. 2004;21(6):877–889.
    1. Saito S, Nakano M. Nitric oxide production by peritoneal macrophages of Mycobacterium bovis BCG-infected or non-infected mice: regulatory roles of T lymphocytes and cytokines. Journal of Leukocyte Biology. 1996;59(6):908–915.
    1. Petricevich VL, Alves RCB. Role of cytokines and nitric oxide in the induction of tuberculostatic macrophage functions. Mediators of Inflammation. 2000;9(6):261–269.
    1. Hawkyard SJ, Jackson AM, Prescott S, James K, Chisholm GD. The effect of recombinant cytokines on bladder cancer cells in vitro. Journal of Urology. 1993;150(2):514–518.
    1. Choi S-C, Oh H-M, Park J-S, et al. Soluble factor from murine bladder tumor-2 cell elevates nitric oxide production in macrophages and enhances the taxol-mediated macrophage cytotoxicity on tumor cells. Cancer Investigation. 2003;21(5):708–719.
    1. O’Donnell MA, Luo Y, Hunter SE, Chen X, Hayes LL, Clinton SK. The essential role of interferon-γ during interleukin-12 therapy for murine transitional cell carcinoma of the bladder. Journal of Urology. 2004;171(3):1336–1342.
    1. Ware CF, VanArsdale S, VanArsdale TL. Apoptosis mediated by the TNF-related cytokine and receptor families. Journal of Cellular Biochemistry. 1996;60(1):47–55.
    1. Laster SM, Wood JG, Gooding LR. Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. Journal of Immunology. 1988;141(8):2629–2634.
    1. Umansky V, Schirrmacher V. Nitric oxide-induced apoptosis in tumor cells. Advances in Cancer Research. 2001;82:107–131.
    1. Greent SJ, Scheller LF, Marletta MA, et al. Nitric Oxide: cytokine-regulation of nitric oxide in host resistance to intracellular pathogens. Immunology Letters. 1994;43(1-2):87–94.
    1. Kindler V, Sappino A-P, Grau GE, Piguet P-F, Vassalli P. The inducing role of tumor necrosis factor in the development of bactericidal granulomas during BCG infection. Cell. 1989;56(5):731–740.
    1. Zhou A, Chen Z, Rummage JA, et al. Exogenous interferon-γ induces endogenous synthesis of interferon-α and -β by murine macrophages for induction of nitric oxide synthase. Journal of Interferon and Cytokine Research. 1995;15(10):897–904.
    1. Huguenin S, Vacherot F, Fleury-Feith J, et al. Evaluation of the antitumoral potential of different nitric oxide-donating non-steroidal anti-inflammatory drugs (NO-NSAIDs) on human urological tumor cell lines. Cancer Letters. 2005;218(2):163–170.
    1. Morcos E, Jansson OT, Adolfsson J, Kratz G, Peter Wiklund N. Endogenously formed nitric oxide modulates cell growth in bladder cancer cell lines. Urology. 1999;53(6):1252–1257.
    1. Jansson OT, Morcos E, Brundin L, et al. The role of nitric oxide in bacillus Calmette-Guérin mediated anti-tumour effects in human bladder cancer. British Journal of Cancer. 1998;78(5):588–592.
    1. 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. Clinical and Experimental Immunology. 2002;127(1):20–26.
    1. De Waal Malefyt R, Abrams J, Bennett B, Figdor CG, De Vries JE. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. Journal of Experimental Medicine. 1991;174(5):1209–1220.
    1. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O’Garra A. IL-10 inhibits cytokine production by activated macrophages. Journal of Immunology. 1991;147(11):3815–3822.
    1. Cenci E, Romani L, Mencacci A, et al. Interleukin-4 and interleukin-10 inhibit nitric oxide-dependent macrophage killing of Candida albicans. European Journal of Immunology. 1993;23(5):1034–1038.
    1. Bogdan C, Vodovotz Y, Nathan C. Macrophage deactivation by interleukin 10. Journal of Experimental Medicine. 1991;174(6):1549–1555.
    1. Chomarat P, Banchereau J, Davoust J, Palucka AK. IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nature Immunology. 2000;1(6):510–514.

Source: PubMed

3
Abonnieren