Complement-dependent modulation of antitumor immunity following radiation therapy

Cell Reports

Volumn 8, Issue 3, 2014, Pages 818-830

  Elvington, Michelle ^a   Scheiber, Melissa ^a   Yang, Xiaofeng ^a   Lyons, Katherine ^a   Jacqmin, Dustin ^a   Wadsworth, Casey ^a   Marshall, David ^a   Vanek, Kenneth ^a   Tomlinson, Stephen ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; COMPLEMENT COMPONENT C3D; COMPLEMENT COMPONENT C5A; COMPLEMENT INHIBITOR; CR2 CRRY; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 6; UNCLASSIFIED DRUG; CR2-CRRY FUSION PROTEIN, MOUSE; HYBRID PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER PREVENTION; CANCER RADIOTHERAPY; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELL TRANSPORT; CELLULAR IMMUNITY; COMPLEMENT ACTIVATION; COMPLEMENT INHIBITION; COMPLEMENT SYSTEM; CONTROLLED STUDY; DENDRITIC CELL; DRUG BINDING; DRUG EFFECT; IMMUNOMODULATION; LONG TERM SURVIVAL; LOW ENERGY RADIATION; MALE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NATURAL KILLER CELL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SUBCUTANEOUS T CELL LYMPHOMA; SUPPRESSOR CELL; SURVIVAL TIME; THERAPY EFFECT; TREATMENT DURATION; TREATMENT OUTCOME; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR RECURRENCE; TUMOR VOLUME; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; IMMUNOLOGY; LYMPHOMA; PATHOLOGY; SUBCUTANEOUS TISSUE; T LYMPHOCYTE; TUMOR CELL LINE;

MURINAE; MUS;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; COMPLEMENT ACTIVATION; COMPLEMENT C3D; COMPLEMENT INACTIVATING AGENTS; DENDRITIC CELLS; IMMUNOMODULATION; LYMPHOMA; MICE; MICE, INBRED C57BL; NEUTROPHIL INFILTRATION; RECOMBINANT FUSION PROTEINS; SUBCUTANEOUS TISSUE; T-LYMPHOCYTES;

EID: 84924599036     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.06.051     Document Type: Article

References (46)

1. Atkinson, C., Song, H., Lu, B., Qiao, F., Burns, T.A., Holers, V.M., Tsokos, G.C., and Tomlinson, S. (2005). Targeted complement inhibition by C3d recognition ameliorates tissue injury without apparent increase in susceptibility to infection. J. Clin. Invest. 115, 2444-2453.
2. Atkinson, C., Qiao, F., Song, H., Gilkeson, G.S., and Tomlinson, S. (2008). Lowdose targeted complement inhibition protects against renal disease and other manifestations of autoimmune disease in MRL/lpr mice. J. Immunol. 180, 1231-1238.
3. Atkinson, C., Varela, J.C., and Tomlinson, S. (2009). Complement-dependent inflammation and injury in a murine model of brain dead donor hearts. Circ. Res. 105, 1094-1101.
4. Burnette, B.C., Liang, H., Lee, Y., Chlewicki, L., Khodarev, N.N., Weichselbaum, R.R., Fu, Y.X., and Auh, S.L. (2011). The efficacy of radiotherapy relies upon induction of type i interferon-dependent innate and adaptive immunity. Cancer Res. 71, 2488-2496.
5. Chen, Y., Park, Y.B., Patel, E., and Silverman, G.J. (2009). IgM antibodies to apoptosis-associated determinants recruit C1q and enhance dendritic cell phagocytosis of apoptotic cells. J. Immunol. 182, 6031-6043.
6. Corrales, L., Ajona, D., Rafail, S., Lasarte, J.J., Riezu-Boj, J.I., Lambris, J.D., Rouzaut, A., Pajares, M.J., Montuenga, L.M., and Pio, R. (2012). Anaphylatoxin C5a creates a favorable microenvironment for lung cancer progression. J. Immunol. 189, 4674-4683.
7. Daley, J.M., Thomay, A.A., Connolly, M.D., Reichner, J.S., and Albina, J.E. (2008). Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 83, 64-70.
8. Demaria, S., and Formenti, S.C. (2012). Role of T lymphocytes in tumor response to radiotherapy. Front Oncol 2, 95.
9. Dewan, M.Z., Galloway, A.E., Kawashima, N., Dewyngaert, J.K., Babb, J.S., Formenti, S.C., and Demaria, S. (2009). Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin. Cancer Res. 15, 5379-5388.
10. Dovedi, S.J., Melis, M.H., Wilkinson, R.W., Adlard, A.L., Stratford, I.J., Honeychurch, J., and Illidge, T.M. (2013). Systemic delivery of a TLR7 agonist in combination with radiation primes durable antitumor immune responses in mouse models of lymphoma. Blood 121, 251-259.
11. Elvington, M., Huang, Y., Morgan, B.P., Qiao, F., van Rooijen, N., Atkinson, C., and Tomlinson, S. (2012). A targeted complement-dependent strategy to improve the outcome of mAb therapy, and characterization in a murine model of metastatic cancer. Blood 119, 6043-6051.
12. Emmerich, J., Mumm, J.B., Chan, I.H., LaFace, D., Truong, H., McClanahan, T., Gorman, D.M., and Oft, M. (2012). IL-10 directly activates and expands tumor-resident CD8(+) T cells without de novo infiltration from secondary lymphoid organs. Cancer Res. 72, 3570-3581.
13. Fadok, V.A., Bratton, D.L., Konowal, A., Freed, P.W., Westcott, J.Y., and Henson, P.M. (1998). Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest. 101, 890-898.
14. Finkelstein, S.E., and Fishman, M. (2012). Clinical opportunities in combining immunotherapy with radiation therapy. Front Oncol 2, 169.
15. Fridlender, Z.G., and Albelda, S.M. (2012). Tumor-associated neutrophils: friend or foe? Carcinogenesis 33, 949-955.
16. Gallucci, S., Lolkema, M., and Matzinger, P. (1999). Natural adjuvants: endogenous activators of dendritic cells. Nat. Med. 5, 1249-1255.
17. Ganem, G., Cartron, G., Girinsky, T., Haas, R.L., Cosset, J.M., and Solal-Celigny, P. (2010). Localized low-dose radiotherapy for follicular lymphoma: history, clinical results, mechanisms of action, and future outlooks. Int. J. Radiat. Oncol. Biol. Phys. 78, 975-982.
18. Gershov, D., Kim, S., Brot, N., and Elkon, K.B. (2000). C-Reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J. Exp. Med. 192, 1353-1364.
19. Godau, J., Heller, T., Hawlisch, H., Trappe, M., Howells, E., Best, J., Zwirner, J., Verbeek, J.S., Hogarth, P.M., Gerard, C., et al. (2004). C5a initiates the inflammatory cascade in immune complex peritonitis. J. Immunol. 173, 3437-3445.
20. Golden, E.B., Pellicciotta, I., Demaria, S., Barcellos-Hoff, M.H., and Formenti, S.C. (2012). The convergence of radiation and immunogenic cell death signaling pathways. Front Oncol 2, 88.
21. Hodge, J.W., Guha, C., Neefjes, J., and Gulley, J.L. (2008). Synergizing radiation therapy and immunotherapy for curing incurable cancers. Opportunities and challenges. Oncology (Williston Park) 22, 1064-1070, discussion 1075, 1080-1081, 1084.
22. Huang, S., Xie, K., Bucana, C.D., Ullrich, S.E., and Bar-Eli, M. (1996). Interleukin 10 suppresses tumor growth and metastasis of human melanoma cells: potential inhibition of angiogenesis. Clin. Cancer Res. 2, 1969-1979.
23. Kemper, C., Mitchell, L.M., Zhang, L., and Hourcade, D.E. (2008). The complement protein properdin binds apoptotic T cells and promotes complement activation and phagocytosis. Proc. Natl. Acad. Sci. USA 105, 9023-9028.
24. Kepp, O., Tesniere, A., Schlemmer, F., Michaud, M., Senovilla, L., Zitvogel, L., and Kroemer, G. (2009). Immunogenic cell death modalities and their impact on cancer treatment. Apoptosis 14, 364-375.
25. Korb, L.C., and Ahearn, J.M. (1997). C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J. Immunol. 158, 4525-4528.
26. Kubota, T., Niwa, R., Satoh, M., Akinaga, S., Shitara, K., and Hanai, N. (2009). Engineered therapeutic antibodies with improved effector functions. Cancer Sci. 100, 1566-1572.
27. Kundu, N., and Fulton, A.M. (1997). Interleukin-10 inhibits tumor metastasis, downregulates MHC class I, and enhances NK lysis. Cell. Immunol. 180, 55-61.
28. Kundu, N., Beaty, T.L., Jackson, M.J., and Fulton, A.M. (1996). Antimetastatic and antitumor activities of interleukin 10 in a murine model of breast cancer. J. Natl. Cancer Inst. 88, 536-541.
29. Laan, M., Cui, Z.H., Hoshino, H., Lötvall, J., Sjöstrand, M., Gruenert, D.C., Skoogh, B.E., and Lindén, A. (1999). Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J. Immunol. 162, 2347-2352.
30. Lee, Y., Auh, S.L., Wang, Y., Burnette, B., Wang, Y., Meng, Y., Beckett, M., Sharma, R., Chin, R., Tu, T., et al. (2009). Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: changing strategies for cancer treatment. Blood 114, 589-595.
31. Lugade, A.A., Moran, J.P., Gerber, S.A., Rose, R.C., Frelinger, J.G., and Lord, E.M. (2005). Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J. Immunol. 174, 7516-7523.
32. Markiewski, M.M., DeAngelis, R.A., Benencia, F., Ricklin-Lichtsteiner, S.K., Koutoulaki, A., Gerard, C., Coukos, G., and Lambris, J.D. (2008). Modulation of the antitumor immune response by complement. Nat. Immunol. 9, 1225-1235.
33. Mevorach, D., Mascarenhas, J.O., Gershov, D., and Elkon, K.B. (1998). Complement-dependent clearance of apoptotic cells by human macrophages. J. Exp. Med. 188, 2313-2320.
34. Miyamoto, M., Prause, O., Sjöstrand, M., Laan, M., Lötvall, J., and Lindén, A. (2003). Endogenous IL-17 as a mediator of neutrophil recruitment caused by endotoxin exposure in mouse airways. J. Immunol. 170, 4665-4672.
35. Mueller, M., Herzog, C., Larmann, J., Schmitz, M., Hilfiker-Kleiner, D., Gessner, J.E., and Theilmeier, G. (2013). The receptor for activated complement factor 5 (C5aR) conveys myocardial ischemic damage by mediating neutrophil transmigration. Immunobiology 218, 1131-1138.
36. Mulé, J.J., McIntosh, J.K., Jablons, D.M., and Rosenberg, S.A. (1990). Antitumor activity of recombinant interleukin 6 in mice. J. Exp. Med. 171, 629-636.
37. Navratil, J.S., Watkins, S.C., Wisnieski, J.J., and Ahearn, J.M. (2001). The globular heads of C1q specifically recognize surface blebs of apoptotic vascular endothelial cells. J. Immunol. 166, 3231-3239.
38. Nunez-Cruz, S., Gimotty, P.A., Guerra, M.W., Connolly, D.C., Wu, Y.Q., DeAngelis, R.A., Lambris, J.D., Coukos, G., and Scholler, N. (2012). Genetic and pharmacologic inhibition of complement impairs endothelial cell function and ablates ovarian cancer neovascularization. Neoplasia 14, 994-1004.
39. Ogden, C.A., deCathelineau, A., Hoffmann, P.R., Bratton, D., Ghebrehiwet, B., Fadok, V.A., and Henson, P.M. (2001). C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194, 781-795.
40. Peng, Y., Martin, D.A., Kenkel, J., Zhang, K., Ogden, C.A., and Elkon, K.B. (2007). Innate and adaptive immune response to apoptotic cells. J. Autoimmun. 29, 303-309.
41. Pio, R., Corrales, L., and Lambris, J.D. (2014). The role of complement in tumor growth. Adv. Exp. Med. Biol. 772, 229-262.
42. Postow, M.A., Callahan, M.K., Barker, C.A., Yamada, Y., Yuan, J., Kitano, S., Mu, Z., Rasalan, T., Adamow, M., Ritter, E., et al. (2012). Immunologic correlates of the abscopal effect in a patient with melanoma. N. Engl. J. Med. 366, 925-931.
43. Silverman, G.J., Grönwall, C., Vas, J., and Chen, Y. (2009). Natural autoantibodies to apoptotic cell membranes regulate fundamental innate immune functions and suppress inflammation. Discov. Med. 8, 151-156.
44. Song, H., He, C., Knaak, C., Guthridge, J.M., Holers, V.M., and Tomlinson, S. (2003). Complement receptor 2-mediated targeting of complement inhibitors to sites of complement activation. J. Clin. Invest. 111, 1875-1885.
45. Suttmann, H., Riemensberger, J., Bentien, G., Schmaltz, D., Stöckle, M., Jocham, D., Böhle, A., and Brandau, S. (2006). Neutrophil granulocytes are required for effective Bacillus Calmette-Guérin immunotherapy of bladder cancer and orchestrate local immune responses. Cancer Res. 66, 8250-8257.
46. Tenner, A.J. (1998). C1q receptors: regulating specific functions of phagocytic cells. Immunobiology 199, 250-264.