Trastuzumab upregulates expression of HLA-ABC and T cell costimulatory molecules through engagement of natural killer cells and stimulation of IFNγ secretion

OncoImmunology

Volumn 5, Issue 4, 2016, Pages

  Chaganty, Bharat K R ^a,b   Lu, Yang ^a   Qiu, Songbo ^a   Somanchi, Srinivas S ^a   Lee, Dean A ^a,b   Fan, Zhen ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

HER2; HLA ABC; IFN ; MHC I; PBMC

Indexed keywords

B7 ANTIGEN; CD86 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GAMMA INTERFERON; HLA ANTIGEN; SMALL INTERFERING RNA; T LYMPHOCYTE RECEPTOR; TRASTUZUMAB;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; UPREGULATION; WESTERN BLOTTING;

EID: 84962784541     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1100790     Document Type: Article

References (40)

1. D.J.Slamon. Proto-oncogenes and human cancers ; editorial. N Engl J Med 1987; 317:955-7; PMID:3627214; http://dx.doi.org/10.1056/NEJM198710083171509
2. D.J.Slamon, G.M.Clark, S.G.Wong, W.J.Levin, A.Ullrich, W.L.McGuire. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987; 235:177-82; PMID:3798106; http://dx.doi.org/10.1126/science.3798106
3. G.N.Hortobagyi. Trastuzumab in the treatment of breast cancer. N Engl J Med 2005; 353:1734-6; PMID:16236745; http://dx.doi.org/10.1056/NEJMe058196
4. C.A.Hudis. Trastuzumab–mechanism of action and use in clinical practice. N Engl J Med 2007; 357:39-51; PMID:17611206; http://dx.doi.org/10.1056/NEJMra043186
5. R.Nahta, D.Yu, M.C.Hung, G.N.Hortobagyi, F.J.Esteva. Mechanisms of disease: understanding resistance to HER2-targeted therapy in human breast cancer. Nat Clin Pract Oncol 2006; 3:269-80; PMID:16683005; http://dx.doi.org/10.1038/ncponc0509
6. J.Baselga, L.Norton, J.Albanell, Y.M.Kim, J.Mendelsohn. Recombinant humanized anti-HER2 antibody (Herceptin) enhances the antitumor activity of paclitaxel and doxorubicin against HER2/neu overexpressing human breast cancer xenografts. Cancer Res 1998; 58:2825-31; PMID:9661897
7. M.A.Cobleigh, C.L.Vogel, D.Tripathy, N.J.Robert, S.Scholl, L.Fehrenbacher, J.M.Wolter, V.Paton, S.Shak, G.Lieberman et al. Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J Clin Oncol 1999; 17:2639-48; PMID:10561337
8. K.Liang, Y.Lu, W.Jin, K.K.Ang, L.Milas, Z.Fan. Sensitization of breast cancer cells to radiation by trastuzumab. Mol Cancer Ther 2003; 2:1113-20; PMID:14617784
9. J.Jacob, L.Belin, J.Y.Pierga, A.Gobillion, A.Vincent-Salomon, R.Dendale, P.Beuzeboc, F.Campana, A.Fourquet, Y.M.Kirova. Concurrent administration of trastuzumab with locoregional breast radiotherapy: long-term results of a prospective study. Breast Cancer Res Treat 2014; 148:345-53; PMID:25318926; http://dx.doi.org/10.1007/s10549-014-3166-5
10. R.A.Clynes, T.L.Towers, L.G.Presta, J.V.Ravetch. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med 2000; 6:443-6; PMID:10742152; http://dx.doi.org/10.1038/74704
11. L.Arnould, M.Gelly, F.Penault-Llorca, L.Benoit, F.Bonnetain, C.Migeon, V.Cabaret, V.Fermeaux, P.Bertheau, J.Garnier et al. Trastuzumab-based treatment of HER2-positive breast cancer: an antibody-dependent cellular cytotoxicity mechanism? Br J Cancer 2006; 94:259-67; PMID:16404427; http://dx.doi.org/10.1038/sj.bjc.6602930
12. S.Park, Z.Jiang, E.D.Mortenson, L.Deng, O.Radkevich-Brown, X.Yang, H.Sattar, Y.Wang, N.K.Brown, M.Greene et al. The therapeutic effect of anti-HER2/neu antibody depends on both innate and adaptive immunity. Cancer Cell 2010; 18:160-70; PMID:20708157; http://dx.doi.org/10.1016/j.ccr.2010.06.014
13. S.Loi. Tumor-infiltrating lymphocytes, breast cancer subtypes and therapeutic efficacy. Oncoimmunology 2013; 2:e24720; PMID:24073365; http://dx.doi.org/10.4161/onci.24720
14. P.Savas, S.Loi. Investigating the positive relationship between tumor-infiltrating lymphocytes and trastuzumab therapy. Immunotherapy 2014; 6:803-5; PMID:25290412; http://dx.doi.org/10.2217/imt.14.60
15. A.Beano, E.Signorino, A.Evangelista, D.Brusa, M.Mistrangelo, M.A.Polimeni, R.Spadi, M.Donadio, L.Ciuffreda, L.Matera. Correlation between NK function and response to trastuzumab in metastatic breast cancer patients. J Transl Med 2008; 6:25; PMID:18485193; http://dx.doi.org/10.1186/1479-5876-6-25
16. S.Ladoire, L.Arnould, G.Mignot, L.Apetoh, C.Rébé, F.Martin, P.Fumoleau, B.Coudert, F.Ghiringhelli. T-bet expression in intratumoral lymphoid structures after neoadjuvant trastuzumab plus docetaxel for HER2-overexpressing breast carcinoma predicts survival. Br J Cancer 2011; 105:366-71; PMID:21750556; http://dx.doi.org/10.1038/bjc.2011.261
17. C.Meyer zum Buschenfelde, C.Hermann, B.Schmidt, C.Peschel, H.Bernhard. Antihuman epidermal growth factor receptor 2 (HER2) monoclonal antibody trastuzumab enhances cytolytic activity of class I-restricted HER2-specific T lymphocytes against HER2-overexpressing tumor cells. Cancer Res 2002; 62:2244-7; PMID:11956077
18. T.Cabrera, P.Stern, F.Garrido. HLA and cancer. In A.C.Ochoa (ed.), Mechanisms of tumor escape from the immune response, 1st ed, London: Taylor & Francis, 2003: 1-17.
19. L.K.Fischer. On naming H2 haplotypes: functional significance of MHC class Ib alleles. Immunogenetics 1997; 46:53-62; PMID:9148789; http://dx.doi.org/10.1007/s002510050242
20. A.Choudhury, J.Charo, S.K.Parapuram, R.C.Hunt, D.M.Hunt, B.Seliger, R.Kiessling. Small interfering RNA (siRNA) inhibits the expression of the Her2/neu gene, upregulates HLA class I and induces apoptosis of Her2/neu positive tumor cell lines. Int J Cancer 2004; 108:71-7; PMID:14618618; http://dx.doi.org/10.1002/ijc.11497
21. F.Herrmann, H.A.Lehr, I.Drexler, G.Sutter, J.Hengstler, U.Wollscheid, B.Seliger. HER-2/neu-mediated regulation of components of the MHC class I antigen-processing pathway. Cancer Res 2004; 64:215-20; PMID:14729627; http://dx.doi.org/10.1158/0008-5472.CAN-2522-2
22. M.Inoue, K.Mimura, S.Izawa, K.Shiraishi, A.Inoue, S.Shiba, M.Watanabe, T.Maruyama, Y.Kawaguchi, S.Inoue et al. Expression of MHC Class I on breast cancer cells correlates inversely with HER2 expression. Oncoimmunology 2012; 1:1104-10; PMID:23170258; http://dx.doi.org/10.4161/onci.21056
23. J.Li, Y.Yang, H.Inoue, M.Mori, T.Akiyoshi. The expression of costimulatory molecules CD80 and CD86 in human carcinoma cell lines: its regulation by interferon gamma and interleukin-10. Cancer Immunol Immunother 1996; 43:213-9; PMID:9003466; http://dx.doi.org/10.1007/s002620050324
24. Z.Zheng, M.Takahashi, S.Aoki, K.Toba, A.Liu, Y.Osman, H.Takahashi, N.Tsukada, N.Suzuki, K.Nikkuni et al. Expression patterns of costimulatory molecules on cells derived from human hematological malignancies. J Exp Clin Cancer Res 1998; 17:251-8; PMID:9894758
25. C.C.Benz, G.K.Scott, J.C.Sarup, R.M.Johnson, D.Tripathy, E.Coronado, H.M.Shepard, C.K.Osborne. Estrogen-dependent, tamoxifen-resistant tumorigenic growth of MCF-7 cells transfected with HER2/neu. Breast Cancer Res Treat 1992; 24:85-95; PMID:8095168; http://dx.doi.org/10.1007/BF01961241
26. K.Liang, F.J.Esteva, C.Albarracin, K.Stemke-Hale, Y.Lu, G.Bianchini, C.Y.Yang, Y.Li, X.Li, C.T.Chen et al. Recombinant human erythropoietin antagonizes trastuzumab treatment of breast cancer cells via Jak2-mediated Src activation and PTEN inactivation. Cancer Cell 2010; 18:423-35; PMID:21075308; http://dx.doi.org/10.1016/j.ccr.2010.10.025
27. W.Min, J.S.Pober, D.R.Johnson. Kinetically coordinated induction of TAP1 and HLA class I by IFN-gamma: the rapid induction of TAP1 by IFN-gamma is mediated by Stat1 alpha. J Immunol 1996; 156:3174-83; PMID:8617938
28. M.Scaltriti, C.Verma, M.Guzman, J.Jimenez, J.L.Parra, K.Pedersen, D.J.Smith, S.Landolfi, S.Ramon y Cajal, J.Arribas et al. Lapatinib, a HER2 tyrosine kinase inhibitor, induces stabilization and accumulation of HER2 and potentiates trastuzumab-dependent cell cytotoxicity. Oncogene 2009; 28:803-14; PMID:19060928; http://dx.doi.org/10.1038/onc.2008.432
29. K.Kono, E.Sato, H.Naganuma, A.Takahashi, K.Mimura, H.Nukui, H.Fujii. Trastuzumab (Herceptin) enhances class I-restricted antigen presentation recognized by HER-2/neu-specific T cytotoxic lymphocytes. Clin Cancer Res 2004; 10:2538-44; PMID:15073134; http://dx.doi.org/10.1158/1078-0432.CCR-03-0424
30. Y.Shi, X.Fan, W.Meng, H.Deng, N.Zhang, Z.An. Engagement of immune effector cells by trastuzumab induces HER2/ERBB2 downregulation in cancer cells through STAT1 activation. Breast Cancer Res 2014; 16:R33; PMID:24693969; http://dx.doi.org/10.1186/bcr3637
31. S.Carrel, A.Schmidt-Kessen, L.Giuffre. Recombinant interferon-gamma can induce the expression of HLA-DR and -DC on DR-negative melanoma cells and enhance the expression of HLA-ABC and tumor-associated antigens. Eur J Immunol 1985; 15:118-23; PMID:3918869; http://dx.doi.org/10.1002/eji.1830150204
32. J.F.Giguere, S.Bounou, J.S.Paquette, J.Madrenas, M.J.Tremblay. Insertion of host-derived costimulatory molecules CD80 (B7.1) and CD86 (B7.2) into human immunodeficiency virus type 1 affects the virus life cycle. J Virol 2004; 78:6222-32; PMID:15163715; http://dx.doi.org/10.1128/JVI.78.12.6222-6232.2004
33. T.Maruyama, K.Mimura, E.Sato, M.Watanabe, Y.Mizukami, Y.Kawaguchi, T.Ando, H.Kinouchi, H.Fujii, K.Kono. Inverse correlation of HER2 with MHC class I expression on oesophageal squamous cell carcinoma. Br J Cancer 2010; 103:552-9; PMID:20628381; http://dx.doi.org/10.1038/sj.bjc.6605772
34. K.Mimura, T.Ando, I.Poschke, D.Mougiakakos, C.C.Johansson, J.Ichikawa, R.Okita, M.I.Nishimura, D.Handke, N.Krug et al. T cell recognition of HLA-A2 restricted tumor antigens is impaired by the oncogene HER2. Int J Cancer 2011; 128:390-401; PMID:20715101; http://dx.doi.org/10.1002/ijc.25613
35. K.Mimura, K.Shiraishi, A.Mueller, S.Izawa, L.F.Kua, J.So, W.P.Yong, H.Fujii, B.Seliger, R.Kiessling et al. The MAPK pathway is a predominant regulator of HLA-A expression in esophageal and gastric cancer. J Immunol 2013; 191:6261-72; PMID:24244023; http://dx.doi.org/10.4049/jimmunol.1301597
36. M.Muhlbauer, M.Fleck, C.Schutz, T.Weiss, M.Froh, C.Blank, J.Schölmerich, C.Hellerbrand. PD-L1 is induced in hepatocytes by viral infection and by interferon-alpha and -gamma and mediates T cell apoptosis. J Hepatol 2006; 45:520-8; PMID:16876901; http://dx.doi.org/10.1016/j.jhep.2006.05.007
37. J.Stagg, S.Loi, U.Divisekera, S.F.Ngiow, H.Duret, H.Yagita, M.W.Teng, M.J.Smyth. 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 U S A 2011; 108:7142-7; PMID:21482773; http://dx.doi.org/10.1073/pnas.1016569108
38. H.Lu, K.Liang, Y.Lu, Z.Fan. The anti-EGFR antibody cetuximab sensitizes human head and neck squamous cell carcinoma cells to radiation in part through inhibiting radiation-induced upregulation of HIF-1alpha. Cancer Lett 2012; 322:78-85; PMID:22348829; http://dx.doi.org/10.1016/j.canlet.2012.02.012
39. M.Zhao, D.Sano, C.R.Pickering, S.A.Jasser, Y.C.Henderson, G.L.Clayman, E.M.Sturgis, T.J.Ow, R.Lotan, T.E.Carey et al. Assembly and initial characterization of a panel of 85 genomically validated cell lines from diverse head and neck tumor sites. Clin Cancer Res 2011; 17:7248-64; PMID:21868764; http://dx.doi.org/10.1158/1078-0432.CCR-11-0690
40. A.Beck, T.Wurch, C.Bailly, N.Corvaia. Strategies and challenges for the next generation of therapeutic antibodies. Nat Rev Immunol 2010; 10:345-52; PMID:20414207; http://dx.doi.org/10.1038/nri2747