Lapatinib and doxorubicin enhance the Stat1-dependent antitumor immune response

European Journal of Immunology

Volumn 43, Issue 10, 2013, Pages 2718-2729

  Hannesdóttir, Lára ^a   Tymoszuk, Piotr ^a   Parajuli, Nirmala ^a   Wasmer, Marie Helene ^a   Philipp, Sonja ^a   Daschil, Nina ^a   Datta, Sebak ^a   Koller, Johann Benedikt ^a   Tripp, Christoph H ^a,b   Stoitzner, Patrizia ^a   Müller Holzner, Elisabeth ^a   Wiegers, Gerrit Jan ^a   Sexl, Veronika ^c   Villunger, Andreas ^a   Doppler, Wolfgang ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b Oncotyrol Center for Personalized Cancer Medicine   (Austria)

^c UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

Antitumor immunity; CD8+ T cells; Doxorubicin; Lapatinib; Stat1

Indexed keywords

CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; LAPATINIB; STAT1 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY;

ANTITUMOR IMMUNITY; CD8+ T CELLS; DOXORUBICIN; LAPATINIB; STAT1;

ANIMALS; ANTIGENS, NEOPLASM; BREAST NEOPLASMS; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELLS, CULTURED; CHEMOTAXIS; DISEASE MODELS, ANIMAL; DOXORUBICIN; FEMALE; HUMANS; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; STAT1 TRANSCRIPTION FACTOR;

EID: 84885700363     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242505     Document Type: Article

References (41)

1. Mattarollo, S. R., Loi, S., Duret, H., Ma, Y., Zitvogel, L. and Smyth, M. J., Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res. 2011. 71: 4809-4820.
2. Stagg, J., Loi, S., Divisekera, U., Ngiow, S. F., Duret, H., Yagita, H., Teng, M. W. et al., Anti-ErbB-2 mAb therapy requires type I and II interferons and synergizes with anti-PD-1 or anti-CD137 mAb therapy. Proc. Natl. Acad. Sci. USA 2011. 108: 7142-7147.
3. Ozao-Choy, J., Ma, G., Kao, J., Wang, G. X., Meseck, M., Sung, M., Schwartz, M. et al., The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res. 2009. 69: 2514-2522.
4. Milano, F., Guarriera, M., Rygiel, A. M. and Krishnadath, K. K., Trastuzumab mediated T-cell response against HER-2/neu overexpressing esophageal adenocarcinoma depends on intact antigen processing machinery. PLoS ONE 2010. 5: e12424.
5. Abe, F., Younos, I., Westphal, S., Samson, H., Scholar, E., Dafferner, A., Hoke, T. A. et al., Therapeutic activity of sunitinib for Her2/neu induced mammary cancer in FVB mice. Int. Immunopharmacol. 2010. 10: 140-145.
6. Zitvogel, L., Apetoh, L., Ghiringhelli, F. and Kroemer, G., Immunological aspects of cancer chemotherapy. Nat. Rev. Immunol. 2008. 8: 59-73.
7. Guy, C. T., Webster, M. A., Schaller, M., Parsons, T. J., Cardiff, R. D. and Muller, W. J., Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc. Natl. Acad. Sci. USA 1992. 89: 10578-10582.
8. Worschech, A., Kmieciak, M., Knutson, K. L., Bear, H. D., Szalay, A. A., Wang, E., Marincola, F. M. et al., Signatures associated with rejection or recurrence in HER-2/neu-positive mammary tumors. Cancer Res. 2008. 68: 2436-2446.
9. Abe, F., Dafferner, A. J., Donkor, M., Westphal, S. N., Scholar, E. M., Solheim, J. C., Singh, R. K. et al., Myeloid-derived suppressor cells in mammary tumor progression in FVB Neu transgenic mice. Cancer Immunol. Immunother. 2010. 59: 47-62.
10. Nair, R. E., Kilinc, M. O., Jones, S. A. and Egilmez, N. K., Chronic immune therapy induces a progressive increase in intratumoral T suppressor activity and a concurrent loss of tumor-specific CD8+ T effectors in her-2/neu transgenic mice bearing advanced spontaneous tumors. J. Immunol. 2006. 176: 7325-7334.
11. Ercolini, A. M., Ladle, B. H., Manning, E. A., Pfannenstiel, L. W., Armstrong, T. D., Machiels, J. P., Bieler, J. G. et al., Recruitment of latent pools of high-avidity CD8(+) T cells to the antitumor immune response. J. Exp. Med. 2005. 201: 1591-1602.
12. Bromberg, J., Stat proteins and oncogenesis. J. Clin. Invest. 2002. 109: 1139-1142.
13. Kaplan, D. H., Shankaran, V., Dighe, A. S., Stockert, E., Aguet, M., Old, L. J. and Schreiber, R. D., Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc. Natl. Acad. Sci. USA 1998. 95: 7556-7561.
14. Chan, S. R., Vermi, W., Luo, J., Lucini, L., Rickert, C., Fowler, A. M., Lonardi, S. et al., STAT1-deficient mice spontaneously develop estrogen receptor alpha-positive luminal mammary carcinomas. Breast Cancer Res. 2012. 14: R16.
15. Schneckenleithner, C., Bago-Horvath, Z., Dolznig, H., Neugebauer, N., Kollmann, K., Kolbe, T., Decker, T. et al., Putting the brakes on mammary tumorigenesis: loss of STAT1 predisposes to intraepithelial neoplasias. Oncotarget 2011. 2: 1043-1054.
16. Klover, P. J., Muller, W. J., Robinson, G. W., Pfeiffer, R. M., Yamaji, D. and Hennighausen, L., Loss of STAT1 from mouse mammary epithelium results in an increased neu-induced tumor burden. Neoplasia 2010. 12: 899-905.
17. Raven, J. F., Williams, V., Wang, S., Tremblay, M. L., Muller, W. J., Durbin, J. E. and Koromilas, A. E., Stat1 is a suppressor of ErbB2/Neu-mediated cellular transformation and mouse mammary gland tumor formation. Cell Cycle 2011. 10: 794-804.
18. Widschwendter, A., Tonko-Geymayer, S., Welte, T., Daxenbichler, G., Marth, C. and Doppler, W., Prognostic significance of signal transducer and activator of transcription 1 activation in breast cancer. Clin. Cancer Res. 2002. 8: 3065-3074.
19. Durbin, J. E., Hackenmiller, R., Simon, M. C. and Levy, D. E., Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 1996. 84: 443-450.
20. Thomas, M., Finnegan, C. E., Rogers, K. M., Purcell, J. W., Trimble, A., Johnston, P. G. and Boland, M. P., STAT1: a modulator of chemotherapy-induced apoptosis. Cancer Res. 2004. 64: 8357-8364.
21. Townsend, P. A., Cragg, M. S., Davidson, S. M., McCormick, J., Barry, S., Lawrence, K. M., Knight, R. A. et al., STAT-1 facilitates the ATM activated checkpoint pathway following DNA damage. J. Cell Sci. 2005. 118: 1629-1639.
22. Tanizaki, J., Okamoto, I., Fumita, S., Okamoto, W., Nishio, K. and Nakagawa, K., Roles of BIM induction and survivin downregulation in lapatinib-induced apoptosis in breast cancer cells with HER2 amplification. Oncogene 2011. 30: 4097-4106.
23. Nanni, P., Landuzzi, L., Nicoletti, G., De Giovanni, C., Rossi, I., Croci, S., Astolfi, A. et al., Immunoprevention of mammary carcinoma in HER-2/neu transgenic mice is IFN-gamma and B cell dependent. J. Immunol. 2004. 173: 2288-2296.
24. Han, Y., Guo, Q., Zhang, M., Chen, Z. and Cao, X., CD69+ CD4+ CD25- T cells, a new subset of regulatory T cells, suppress T cell proliferation through membrane-bound TGF-beta 1. J. Immunol. 2009. 182: 111-120.
25. Parajuli, N., Muller-Holzner, E., Bock, G., Werner, E. R., Villunger, A. and Doppler, W., Infiltrating CD11b+CD11c +cells have the potential to mediate inducible nitric oxide synthase-dependent cell death in mammary carcinomas of HER-2/neu transgenic mice. Int. J. Cancer 2010. 126: 896-908.
26. MacDonald, K. P., Palmer, J. S., Cronau, S., Seppanen, E., Olver, S., Raffelt, N. C., Kuns, R. et al., An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue- and tumor-associated macrophages but does not inhibit inflammation. Blood 2010. 116: 3955-3963.
27. Movahedi, K., Laoui, D., Gysemans, C., Baeten, M., Stange, G., Van den Bossche, J., Mack, M. et al., Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 2010. 70: 5728-5739.
28. Quigley, M., Huang, X. and Yang, Y., STAT1 signaling in CD8 T cells is required for their clonal expansion and memory formation following viral infection in vivo. J. Immunol. 2008. 180: 2158-2164.
29. Groom, J. R. and Luster, A. D., CXCR3 in T cell function. Exp. Cell Res. 2011. 317: 620-631.
30. Saha, B., Jyothi Prasanna, S., Chandrasekar, B. and Nandi, D., Gene modulation and immunoregulatory roles of interferon gamma. Cytokine 2010. 50: 1-14.
31. Wendel, M., Galani, I. E., Suri-Payer, E. and Cerwenka, A., Natural killer cell accumulation in tumors is dependent on IFN-gamma and CXCR3 ligands. Cancer Res. 2008. 68: 8437-8445.
32. Pilz, A., Kratky, W., Stockinger, S., Simma, O., Kalinke, U., Lingnau, K., von Gabain, A. et al., Dendritic cells require STAT-1 phosphorylated at its transactivating domain for the induction of peptide-specific CTL. J. Immunol. 2009. 183: 2286-2293.
33. Park, S., Jiang, Z., Mortenson, E. D., Deng, L., Radkevich-Brown, O., Yang, X., Sattar, H. et al., The therapeutic effect of anti-HER2/neu antibody depends on both innate and adaptive immunity. Cancer Cell 2010. 18: 160-170.
34. Ma, Y., Aymeric, L., Locher, C., Kroemer, G. and Zitvogel, L., The dendritic cell-tumor cross-talk in cancer. Curr. Opin. Immunol. 2011. 23: 146-152.
35. Ciampricotti, M., Hau, C. S., Doornebal, C. W., Jonkers, J. and de Visser, K. E., Chemotherapy response of spontaneous mammary tumors is independent of the adaptive immune system. Nat. Med. 2012. 18: 344-346.
36. Gabrilovich, D. I. and Nagaraj, S., Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009. 9: 162-174.
37. Peranzoni, E., Zilio, S., Marigo, I., Dolcetti, L., Zanovello, P., Mandruzzato, S. and Bronte, V., Myeloid-derived suppressor cell heterogeneity and subset definition. Curr. Opin. Immunol. 2010. 22: 238-244.
38. Biswas, S. K. and Mantovani, A., Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 2010. 11: 889-896.
39. Weigelt, B., Lo, A. T., Park, C. C., Gray, J. W. and Bissell, M. J., HER2 signaling pathway activation and response of breast cancer cells to HER2-targeting agents is dependent strongly on the 3D microenvironment. Breast Cancer Res. Treat. 2010. 122: 35-43.
40. Parajuli, N. and Doppler, W., Precision-cut slice cultures of tumors from MMTV-neu mice for the study of the ex vivo response to cytokines and cytotoxic drugs. In Vitro Cell. Dev. Biol. Anim. 2009. 45: 442-450.
41. Berlato, C. and Doppler, W., Selective response to insulin versus insulin-like growth factor-I and -II and up-regulation of insulin receptor splice variant B in the differentiated mouse mammary epithelium. Endocrinology 2009. 150: 2924-2933.