Combination of IFNα and poly-I: C reprograms bladder cancer microenvironment for enhanced CTL attraction

Journal for ImmunoTherapy of Cancer

Volumn 3, Issue 1, 2015, Pages

  Muthuswamy, Ravikumar ^a   Wang, Liwen ^a   Pitteroff, Jamie ^a   Gingrich, Jeffrey R ^b   Kalinski, Pawel ^a,b,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

BCG; Bladder cancer; Chemokines; Effector T cells; IFN ; Immunomodulation; Poly I :C; Regulatory T cells; TLR3; Tumor microenvironment

Indexed keywords

ALPHA INTERFERON; BCG VACCINE; CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANZYME B; INTERLEUKIN 8; MACROPHAGE DERIVED CHEMOKINE; MESSENGER RNA; POLYINOSINIC POLYCYTIDYLIC ACID; RANTES;

ARTICLE; BLADDER CANCER; BLADDER CANCER CELL LINE; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER TISSUE; CD8+ T LYMPHOCYTE; CELL MIGRATION; CHEMOTAXIS; CLINICAL TRIAL (TOPIC); COCULTURE; CONFOCAL MICROSCOPY; CYTOTOXIC T LYMPHOCYTE; DRUG EFFICACY; EFFECTOR CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; FEMALE; FIBROBLAST; GRANULOCYTE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; MACROPHAGE; MALE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SUPPRESSOR CELL; TUMOR MICROENVIRONMENT; UPREGULATION;

EID: 84977156548     PISSN: None     EISSN: 20511426     Source Type: Journal    
DOI: 10.1186/s40425-015-0050-8     Document Type: Article

References (44)

1. Gofrit ON, Pode D, Pizov G, Zorn KC, Katz R, Duvdevani M, et al. The natural history of bladder carcinoma in situ after initial response to bacillus Calmette-Guerin immunotherapy. Urol Oncol 2009, 27:258-62. 10.1016/j.urolonc.2007.12.011, 18440839.
2. Herr HW, Morales A. History of bacillus Calmette-Guerin and bladder cancer: an immunotherapy success story. J Urol 2008, 179:53-6. 10.1016/j.juro.2007.08.122, 17997439.
3. Morales A, Eidinger D, Bruce AW. Intracavitary Bacillus Calmette-Guerin in the treatment of superficial bladder tumors. J Urol 1976, 167:891-3. discussion 893-895, 10.1016/S0022-5347(02)80294-4.
4. Zhu S, Tang Y, Li K, Shang Z, Jiang N, Nian X, et al. Optimal schedule of bacillus calmette-guerin for non-muscle-invasive bladder cancer: a meta-analysis of comparative studies. BMC Cancer 2013, 13:332. 10.1186/1471-2407-13-332, 23829273.
5. Fujii H, Arakawa A, Utsumi D, Sumiyoshi S, Yamamoto Y, Kitoh A, et al. CD8+ tumor-infiltrating lymphocytes at primary sites as a possible prognostic factor of cutaneous angiosarcoma. Int J Cancer 2014, 134(10):2393-2402. 10.1002/ijc.28581, 24243586.
6. Nasman A, Romanitan M, Nordfors C, Grun N, Johansson H, Hammarstedt L, et al. Tumor infiltrating CD8+ and Foxp3+ lymphocytes correlate to clinical outcome and human papillomavirus (HPV) status in tonsillar cancer. PLoS One 2012, 7:e38711. 10.1371/journal.pone.0038711, 22701698.
7. Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012, 12:298-306. 10.1038/nrc3245, 22419253.
8. Mahmoud SM, Paish EC, Powe DG, Macmillan RD, Grainge MJ, Lee AH, et al. Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. J Clin Oncol 2011, 29:1949-55. 10.1200/JCO.2010.30.5037, 21483002.
9. Yamada N, Oizumi S, Kikuchi E, Shinagawa N, Konishi-Sakakibara J, Ishimine A, et al. CD8+ tumor-infiltrating lymphocytes predict favorable prognosis in malignant pleural mesothelioma after resection. Cancer Immunol Immunother 2010, 59:1543-9. 10.1007/s00262-010-0881-6, 20567822.
10. Mlecnik B, Tosolini M, Charoentong P, Kirilovsky A, Bindea G, Berger A, et al. Biomolecular network reconstruction identifies T-cell homing factors associated with survival in colorectal cancer. Gastroenterology 2010, 138:1429-40. 10.1053/j.gastro.2009.10.057, 19909745.
11. Dudley ME, Gross CA, Langhan MM, Garcia MR, Sherry RM, Yang JC, et al. CD8+ enriched " young" tumor infiltrating lymphocytes can mediate regression of metastatic melanoma. Clin Cancer Res 2010, 16:6122-31. 10.1158/1078-0432.CCR-10-1297, 20668005.
12. Pages F, Kirilovsky A, Mlecnik B, Asslaber M, Tosolini M, Bindea G, et al. In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol 2009, 27:5944-51. 10.1200/JCO.2008.19.6147, 19858404.
13. Sharma P, Shen Y, Wen S, Yamada S, Jungbluth AA, Gnjatic S, et al. CD8 tumor-infiltrating lymphocytes are predictive of survival in muscle-invasive urothelial carcinoma. Proc Natl Acad Sci U S A 2007, 104:3967-72. 10.1073/pnas.0611618104, 17360461.
14. Piersma SJ, Jordanova ES, van Poelgeest MI, Kwappenberg KM, van der Hulst JM, Drijfhout JW, et al. High number of intraepithelial CD8+ tumor-infiltrating lymphocytes is associated with the absence of lymph node metastases in patients with large early-stage cervical cancer. Cancer Res 2007, 67:354-61. 10.1158/0008-5472.CAN-06-3388, 17210718.
15. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006, 313:1960-4. 10.1126/science.1129139, 17008531.
16. Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, Qian F, et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 2005, 102:18538-43. 10.1073/pnas.0509182102, 16344461.
17. Pages F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 2005, 353:2654-66. 10.1056/NEJMoa051424, 16371631.
18. Prall F, Duhrkop T, Weirich V, Ostwald C, Lenz P, Nizze H, et al. Prognostic role of CD8+ tumor-infiltrating lymphocytes in stage III colorectal cancer with and without microsatellite instability. Hum Pathol 2004, 35:808-16. 10.1016/j.humpath.2004.01.022, 15257543.
19. Muthuswamy R, Berk E, Junecko BF, Zeh HJ, Zureikat AH, Normolle D, et al. NF-kappaB hyperactivation in tumor tissues allows tumor-selective reprogramming of the chemokine microenvironment to enhance the recruitment of cytolytic T effector cells. Cancer Res 2012, 72:3735-43. 10.1158/0008-5472.CAN-11-4136, 22593190.
20. Ohta M, Tanaka F, Yamaguchi H, Sadanaga N, Inoue H, Mori M. The high expression of Fractalkine results in a better prognosis for colorectal cancer patients. Int J Oncol 2005, 26:41-7. 15586223.
21. Harlin H, Meng Y, Peterson AC, Zha Y, Tretiakova M, Slingluff C, et al. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res 2009, 69:3077-85. 10.1158/0008-5472.CAN-08-2281, 19293190.
22. Ohtani H, Jin Z, Takegawa S, Nakayama T, Yoshie O. Abundant expression of CXCL9 (MIG) by stromal cells that include dendritic cells and accumulation of CXCR3+ T cells in lymphocyte-rich gastric carcinoma. J Pathol 2009, 217:21-31. 10.1002/path.2448, 18980207.
23. Venetz D, Ponzoni M, Schiraldi M, Ferreri AJ, Bertoni F, Doglioni C, et al. Perivascular expression of CXCL9 and CXCL12 in primary central nervous system lymphoma: T-cell infiltration and positioning of malignant B cells. Int J Cancer 2010, 127:2300-12. 10.1002/ijc.25236, 20872671.
24. Martinet L, Le Guellec S, Filleron T, Lamant L, Meyer N, Rochaix P, et al. High endothelial venules (HEVs) in human melanoma lesions: Major gateways for tumor-infiltrating lymphocytes. Oncoimmunology 2012, 1:829-39. 10.4161/onci.20492, 23162750.
25. Lanca T, Costa MF, Goncalves-Sousa N, Rei M, Grosso AR, Penido C, et al. Protective role of the inflammatory CCR2/CCL2 chemokine pathway through recruitment of type 1 cytotoxic gammadelta T lymphocytes to tumor beds. J Immunol 2013, 190:6673-80. 10.4049/jimmunol.1300434, 23686489.
26. Katoh H, Wang D, Daikoku T, Sun H, Dey SK, Dubois RN. CXCR2-Expressing Myeloid-Derived Suppressor Cells Are Essential to Promote Colitis-Associated Tumorigenesis. Cancer Cell 2013, 24:631-44. 10.1016/j.ccr.2013.10.009, 24229710.
27. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004, 10:942-9. 10.1038/nm1093, 15322536.
28. Zou L, Barnett B, Safah H, Larussa VF, Evdemon-Hogan M, Mottram P, et al. Bone marrow is a reservoir for CD4 + CD25+ regulatory T cells that traffic through CXCL12/CXCR4 signals. Cancer Res 2004, 64:8451-5. 10.1158/0008-5472.CAN-04-1987, 15548717.
29. Obermajer N, Muthuswamy R, Odunsi K, Edwards RP, Kalinski P. PGE(2)-induced CXCL12 production and CXCR4 expression controls the accumulation of human MDSCs in ovarian cancer environment. Cancer Res 2011, 71:7463-70. 10.1158/0008-5472.CAN-11-2449, 22025564.
30. Obermajer N, Wong JL, Edwards RP, Odunsi K, Moysich K, Kalinski P. PGE(2)-driven induction and maintenance of cancer-associated myeloid-derived suppressor cells. Immunol Investig 2012, 41:635-57. 10.3109/08820139.2012.695417.
31. Reis ST, Leite KR, Piovesan LF, Pontes-Junior J, Viana NI, Abe DK, et al. Increased expression of MMP-9 and IL-8 are correlated with poor prognosis of Bladder Cancer. BMC Urol 2012, 12:18. 10.1186/1471-2490-12-18, 22695075.
32. Svatek RS, Zhao XR, Morales EE, Jha MK, Tseng TY, Hugen CM, et al. Sequential Intravesical Mitomycin plus Bacillus Calmette-Guerin for Non-Muscle-Invasive Urothelial Bladder Carcinoma: Translational and Phase I Clinical Trial. Clin Cancer Res 2015, 21:303-11. 10.1158/1078-0432.CCR-14-1781, 25424854.
33. Yamada H, Luo Y, Matsumoto T, O'Donnell MA. A novel expression of macrophage derived chemokine in human bladder cancer. J Urol 2005, 173:990-5. 10.1097/01.ju.0000155188.04120.f8, 15711363.
34. Nepple KG, Lightfoot AJ, Rosevear HM, O'Donnell MA, Lamm DL. Bacillus Calmette-Guerin with or without interferon alpha-2b and megadose versus recommended daily allowance vitamins during induction and maintenance intravesical treatment of nonmuscle invasive bladder cancer. J Urol 2010, 184:1915-9. 10.1016/j.juro.2010.06.147, 20846688.
35. Lamm D, Brausi M, O'Donnell MA, Witjes JA. Interferon alfa in the treatment paradigm for non-muscle-invasive bladder cancer. Urol Oncol 2014, 32:35. e21-30, 10.1016/j.urolonc.2013.02.010, 23628309.
36. Watchmaker PB, Berk E, Muthuswamy R, Mailliard RB, Urban JA, Kirkwood JM, et al. Independent regulation of chemokine responsiveness and cytolytic function versus CD8+ T cell expansion by dendritic cells. J Immunol 2010, 184:591-7. 10.4049/jimmunol.0902062, 20018619.
37. Vieira PL, de Jong EC, Wierenga EA, Kapsenberg ML, Kalinski P. Development of Th1-inducing capacity in myeloid dendritic cells requires environmental instruction. J Immunol 2000, 164:4507-12. 10.4049/jimmunol.164.9.4507, 10779751.
38. Bisiaux A, Thiounn N, Timsit MO, Eladaoui A, Chang HH, Mapes J, et al. Molecular analyte profiling of the early events and tissue conditioning following intravesical bacillus calmette-guerin therapy in patients with superficial bladder cancer. J Urol 2009, 181:1571-80. 10.1016/j.juro.2008.11.124, 19230924.
39. Mendez-Samperio P, Alba L, Perez A. Mycobacterium bovis bacillus Calmette-Guerin (BCG)-induced CXCL8 production is mediated through PKCalpha-dependent activation of the IKKalphabeta signaling pathway in epithelial cells. Cell Immunol 2007, 245:111-8. 10.1016/j.cellimm.2007.04.005, 17562331.
40. Mendez-Samperio P, Perez A, Rivera L. Mycobacterium bovis Bacillus Calmette-Guerin (BCG)-induced activation of PI3K/Akt and NF-kB signaling pathways regulates expression of CXCL10 in epithelial cells. Cell Immunol 2009, 256:12-8. 10.1016/j.cellimm.2008.12.002, 19181310.
41. Heldwein KA, Liang MD, Andresen TK, Thomas KE, Marty AM, Cuesta N, et al. TLR2 and TLR4 serve distinct roles in the host immune response against Mycobacterium bovis BCG. J Leukoc Biol 2003, 74:277-86. 10.1189/jlb.0103026, 12885945.
42. Barbalat R, Lau L, Locksley RM, Barton GM. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat Immunol 2009, 10:1200-7. 10.1038/ni.1792, 19801985.
43. Liu YC, Simmons DP, Li X, Abbott DW, Boom WH, Harding CV. TLR2 signaling depletes IRAK1 and inhibits induction of type I IFN by TLR7/9. J Immunol 2012, 188:1019-26. 10.4049/jimmunol.1102181, 22227568.
44. Muthuswamy R, Urban J, Lee JJ, Reinhart TA, Bartlett D, Kalinski P. Ability of mature dendritic cells to interact with regulatory T cells is imprinted during maturation. Cancer Res 2008, 68:5972-8. 10.1158/0008-5472.CAN-07-6818, 18632653.