1 alpha, 25-dihydroxylvitamin D3 promotes Bacillus Calmette-Guérin immunotherapy of bladder cancer

Oncotarget

Volumn 4, Issue 12, 2013, Pages 2397-2406

  Hsu, Jong Wei ^a,b   Yin, Peng Nien ^a   Wood, Ronald ^a   Messing, James ^c   Messing, Edward ^a   Lee, Yi Fen ^a,b  

^a UNIVERSITY OF ROCHESTER   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

Bacillus Calmette Gu rin; Bladder cancer; Immunotherapy; Interleukin 8; Vitamin D

Indexed keywords

1 ALPHA, 25 DIHYDROXYLVITAMIN D3; BCG VACCINE; CELL MARKER; COLECALCIFEROL DERIVATIVE; INTERLEUKIN 8; INTERLEUKIN 8 ANTIBODY; N BUTYL N (4 HYDROXYBUTYL)NITROSAMINE; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLADDER CANCER; CANCER CELL; CANCER IMMUNOTHERAPY; CANCER SURVIVAL; CELL MIGRATION; CELL STRAIN; CELL STRAIN THP 1; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG POTENTIATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; MACROPHAGE MIGRATION; MOUSE; NONHUMAN; SURVIVAL TIME;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BCG VACCINE; CALCITRIOL; CELL LINE; DRUG SYNERGISM; FEMALE; HL-60 CELLS; HUMANS; IMMUNOTHERAPY; INTERLEUKIN-8; MACROPHAGES; MICE; URINARY BLADDER NEOPLASMS;

EID: 84891922851     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1494     Document Type: Article

References (49)

1. Jemal A, Siegel R, Xu J and Ward E. Cancer statistics, 2010. CA Cancer J Clin. 2010; 60(5):277-300.
2. Botteman MF, Pashos CL, Redaelli A, Laskin B and Hauser R. The health economics of bladder cancer: a comprehensive review of the published literature. Pharmacoeconomics. 2003; 21(18):1315-1330.
3. Sylvester RJ, van der Meijden AP, Oosterlinck W, Witjes JA, Bouffioux C, Denis L, Newling DW and Kurth K. Predicting recurrence and progression in individual patients with stage Ta T1 bladder cancer using EORTC risk tables: a combined analysis of 2596 patients from seven EORTC trials. Eur Urol. 2006; 49(3):466-465; discussion 475-467.
4. Morales A, Eidinger D and Bruce AW. Intracavitary Bacillus Calmette-Guerin in the treatment of superficial bladder tumors. The Journal of urology. 1976; 116(2):180-183.
5. Kresowik TP and Griffith TS. Bacillus Calmette-Guerin immunotherapy for urothelial carcinoma of the bladder. Immunotherapy. 2009; 1(2):281-288.
6. Herr HW, Schwalb DM, Zhang ZF, Sogani PC, Fair WR, Whitmore WF, Jr. and Oettgen HF. Intravesical bacillus Calmette-Guerin therapy prevents tumor progression and death from superficial bladder cancer: ten-year follow-up of a prospective randomized trial. J Clin Oncol. 1995; 13(6):1404-1408.
7. Ratliff TL, Palmer JO, McGarr JA and Brown EJ. Intravesical Bacillus Calmette-Guerin therapy for murine bladder tumors: initiation of the response by fibronectin-mediated attachment of Bacillus Calmette-Guerin. Cancer Res. 1987; 47(7):1762-1766.
8. Kuroda K, Brown EJ, Telle WB, Russell DG and Ratliff TL. Characterization of the internalization of bacillus Calmette-Guerin by human bladder tumor cells. J Clin Invest. 1993; 91(1):69-76.
9. de Boer EC, de Jong WH, van der Meijden AP, Steerenberg PA, Witjes F, Vegt PD, Debruyne FM and Ruitenberg EJ. Leukocytes in the urine after intravesical BCG treatment for superficial bladder cancer. A flow cytofluorometric analysis. Urol Res. 1991; 19(1):45-50.
10. Ludwig AT, Moore JM, Luo Y, Chen X, Saltsgaver NA, O'Donnell MA and Griffith TS. Tumor necrosis factor-related apoptosis-inducing ligand: a novel mechanism for Bacillus Calmette-Guerin-induced antitumor activity. Cancer Res. 2004; 64(10):3386-3390.
11. Luo Y, Yamada H, Evanoff DP and Chen X. Role of Th1-stimulating cytokines in bacillus Calmette-Guerin (BCG)-induced macrophage cytotoxicity against mouse bladder cancer MBT-2 cells. Clinical and experimental immunology. 2006; 146(1):181-188.
12. Bettex-Galland M, Studer UE, Walz A, Dewald B and Baggiolini M. Neutrophil-activating peptide-1/interleukin-8 detection in human urine during acute bladder inflammation caused by transurethral resection of superficial cancer and bacillus Calmette-Guerin administration. European urology. 1991; 19(2):171-175.
13. Thalmann GN, Sermier A, Rentsch C, Mohrle K, Cecchini MG and Studer UE. Urinary Interleukin-8 and 18 predict the response of superficial bladder cancer to intravesical therapy with bacillus Calmette-Guerin. The Journal of urology. 2000; 164(6):2129-2133.
14. Rabinowitz R, Smith DS, Tiemann DD and Hudson MA. Urinary interleukin-8/creatinine level as a predictor of response to intravesical bacillus Calmette-Guerin therapy in bladder tumor patients. The Journal of urology. 1997; 158(5):1728-1731; discussion 1731-1722.
15. Yamada H, Matsumoto S, Matsumoto T, Yamada T and Yamashita U. Murine IL-2 secreting recombinant Bacillus Calmette-Guerin augments macrophage-mediated cytotoxicity against murine bladder cancer MBT-2. The Journal of urology. 2000; 164(2):526-531.
16. Brandau S and 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.
17. Messing EM. Words of wisdom. Re: Preexisting BCG-specific T cells improve intravesical immunotherapy for bladder cancer. Eur Urol. 2012; 62(5):935-936.
18. Biot C, Rentsch CA, Gsponer JR, Birkhauser FD, Jusforgues-Saklani H, Lemaitre F, Auriau C, Bachmann A, Bousso P, Demangel C, Peduto L, Thalmann GN and Albert ML. Preexisting BCG-specific T cells improve intravesical immunotherapy for bladder cancer. Sci Transl Med. 2012; 4(137):137ra172.
19. Lamm DL, van der Meijden PM, Morales A, Brosman SA, Catalona WJ, Herr HW, Soloway MS, Steg A and Debruyne FM. Incidence and treatment of complications of bacillus Calmette-Guerin intravesical therapy in superficial bladder cancer. The Journal of urology. 1992; 147(3):596-600.
20. Thalmann GN, Dewald B, Baggiolini M and Studer UE. Interleukin-8 expression in the urine after bacillus Calmette-Guerin therapy: a potential prognostic factor of tumor recurrence and progression. The Journal of urology. 1997; 158(4):1340-1344.
21. Rawls WH, Lamm DL, Lowe BA, Crawford ED, Sarosdy MF, Montie JE, Grossman HB and Scardino PT. Fatal sepsis following intravesical bacillus Calmette-Guerin administration for bladder cancer. The Journal of urology. 1990; 144(6):1328-1330.
22. Nnoaham KE and Clarke A. Low serum vitamin D levels and tuberculosis: a systematic review and meta-analysis. Int J Epidemiol. 2008; 37(1):113-119.
23. Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR, Ochoa MT, Schauber J, Wu K, Meinken C, Kamen DL, Wagner M, Bals R, Steinmeyer A, Zugel U, Gallo RL, et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science. 2006; 311(5768):1770-1773.
24. Sahin MO, Canda AE, Yorukoglu K, Mungan MU, Sade M and Kirkali Z. 1,25 Dihydroxyvitamin D(3) receptor expression in superficial transitional cell carcinoma of the bladder: a possible prognostic factor? Eur Urol. 2005; 47(1):52-57.
25. Mondul AM, Weinstein SJ, Mannisto S, Snyder K, Horst RL, Virtamo J and Albanes D. Serum vitamin D and risk of bladder cancer. Cancer Res. 2010; 70(22):9218-9223.
26. Dancik GM, Ru Y, Owens CR and Theodorescu D. A framework to select clinically relevant cancer cell lines for investigation by establishing their molecular similarity with primary human cancers. Cancer Res. 2011; 71(24):7398-7409.
27. Hsu JW, Yasmin-Karim S, King MR, Wojciechowski JC, Mickelsen D, Blair ML, Ting HJ, Ma WL and Lee YF. Suppression of prostate cancer cell rolling and adhesion to endothelium by 1alpha,25-dihydroxyvitamin D3. The American journal of pathology. 2011; 178(2):872-880.
28. de Reijke TM, Vos PC, de Boer EC, Bevers RF, de Muinck Keizer WH, Kurth KH and Schamhart DH. Cytokine production by the human bladder carcinoma cell line T24 in the presence of bacillus Calmette-Guerin (BCG). Urol Res. 1993; 21(5):349-352.
29. Esuvaranathan K, Alexandroff AB, McIntyre M, Jackson AM, Prescott S, Chisholm GD and James K. Interleukin-6 production by bladder tumors is upregulated by BCG immunotherapy. The Journal of urology. 1995; 154(2 Pt 1):572-575.
30. Suttmann H, Riemensberger J, Bentien G, Schmaltz D, Stockle M, Jocham D, Bohle A and Brandau S. Neutrophil granulocytes are required for effective Bacillus Calmette-Guerin immunotherapy of bladder cancer and orchestrate local immune responses. Cancer Res. 2006; 66(16):8250-8257.
31. Fabriek BO, van Bruggen R, Deng DM, Ligtenberg AJ, Nazmi K, Schornagel K, Vloet RP, Dijkstra CD and van den Berg TK. The macrophage scavenger receptor CD163 functions as an innate immune sensor for bacteria. Blood. 2009; 113(4):887-892.
32. Luo Y and Knudson MJ. Mycobacterium bovis bacillus Calmette-Guerin-induced macrophage cytotoxicity against bladder cancer cells. Clin Dev Immunol. 2010; 2010:357591.
33. Hsu JW, Hsu I, Xu D, Miyamoto H, Liang L, Wu XR, Shyr CR and Chang C. Decreased tumorigenesis and mortality from bladder cancer in mice lacking urothelial androgen receptor. The American journal of pathology. 2013; 182(5):1811-1820.
34. Luo Y, Han R, Evanoff DP and Chen X. Interleukin-10 inhibits Mycobacterium bovis bacillus Calmette-Guerin (BCG)-induced macrophage cytotoxicity against bladder cancer cells. Clinical and experimental immunology. 2010; 160(3):359-368.
35. Zaharoff DA, Hoffman BS, Hooper HB, Benjamin CJ, Jr., Khurana KK, Hance KW, Rogers CJ, Pinto PA, Schlom J and Greiner JW. Intravesical immunotherapy of superficial bladder cancer with chitosan/interleukin-12. Cancer Res. 2009; 69(15):6192-6199.
36. Reece ST, Nasser-Eddine A, Dietrich J, Stein M, Zedler U, Schommer-Leitner S, Ottenhoff TH, Andersen P and Kaufmann SH. Improved long-term protection against Mycobacterium tuberculosis Beijing/W in mice after intra-dermal inoculation of recombinant BCG expressing latency associated antigens. Vaccine. 2011; 29(47):8740-8744.
37. Konety BR, Lavelle JP, Pirtskalaishvili G, Dhir R, Meyers SA, Nguyen TS, Hershberger P, Shurin MR, Johnson CS, Trump DL, Zeidel ML and Getzenberg RH. Effects of vitamin D (calcitriol) on transitional cell carcinoma of the bladder in vitro and in vivo. J Urol. 2001; 165(1):253-258.
38. Ratliff TL. Role of animal models in understanding intravesical therapy with bacille Calmette-Guerin. Clin Infect Dis. 2000; 31 Suppl 3:S106-108.
39. Polly P, Carlberg C, Eisman JA and Morrison NA. Identification of a vitamin D3 response element in the fibronectin gene that is bound by a vitamin D3 receptor homodimer. J Cell Biochem. 1996; 60(3):322-333.
40. de Boer EC, Somogyi L, de Ruiter GJ, de Reijke TM, Kurth KH and Schamhart DH. Role of interleukin-8 in onset of the immune response in intravesical BCG therapy for superficial bladder cancer. Urol Res. 1997; 25(1):31-34.
41. Kumar A, Dubey D, Bansal P, Mandhani A and Naik S. Urinary interleukin-8 predicts the response of standard and low dose intravesical bacillus Calmette-Guerin (modified Danish 1331 strain) for superficial bladder cancer. The Journal of urology. 2002; 168(5):2232-2235.
42. Sagnak L, Ersoy H, Ozok U, Senturk B, Ercil H, Bahar G and Ozturk E. Predictive value of urinary interleukin-8 cutoff point for recurrences after transurethral resection plus induction bacillus Calmette-Guerin treatment in non-muscle-invasive bladder tumors. Clin Genitourin Cancer. 2009; 7(2):E16-23.
43. Cheever MA. Twelve immunotherapy drugs that could cure cancers. Immunol Rev. 2008; 222:357-368.
44. Dodane V, Amin Khan M and Merwin JR. Effect of chitosan on epithelial permeability and structure. Int J Pharm. 1999; 182(1):21-32.
45. Bao BY, Yao J and Lee YF. 1alpha, 25-dihydroxyvitamin D3 suppresses interleukin-8-mediated prostate cancer cell angiogenesis. Carcinogenesis. 2006; 27(9):1883-1893.
46. Larue H, Ayari C, Bergeron A and Fradet Y. Toll-like receptors in urothelial cells-targets for cancer immunotherapy. Nature reviews Urology. 2013; 10(9):537-545.
47. Kawai T and Akira S. Signaling to NF-kappaB by Toll-like receptors. Trends in molecular medicine. 2007; 13(11):460-469.
48. Khoo AL, Chai LY, Koenen HJ, Oosting M, Steinmeyer A, Zuegel U, Joosten I, Netea MG and van der Ven AJ. Vitamin D(3) down-regulates proinflammatory cytokine response to Mycobacterium tuberculosis through pattern recognition receptors while inducing protective cathelicidin production. Cytokine. 2011; 55(2):294-300.
49. Choi KY and Mookherjee N. Multiple immune-modulatory functions of cathelicidin host defense peptides. Frontiers in immunology. 2012; 3:149.