Overexpression of CD85j in TNBC patients inhibits Cetuximab-mediated NK-cell ADCC but can be restored with CD85j functional blockade

European Journal of Immunology

Volumn 45, Issue 5, 2015, Pages 1560-1569

  Roberti, María P ^a   Juliá, Estefanía P ^a   Rocca, Yamila S ^b   Amat, Mora ^c   Bravo, Alicia I ^d   Loza, José ^c   Coló, Federico ^c   Loza, Carlos M ^c   Fabiano, Verónica ^c   Maino, Mercedes ^c   Podhorzer, Ariel ^e   Fainboim, Leonardo ^e   Barrio, María M ^a   Mordoh, José ^a,b,c   Levy, Estrella M ^a  

^a CIO FUCA   (Argentina)

^b FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^c INSTITUTO ALEXANDER FLEMING   (Argentina)

^d Hospital Eva Peron   (Argentina)

^e HOSPITAL DE CLÍNICAS JOSÉ DE SAN MARTÍN   (Argentina)

Author keywords

ADCC; CD85j; Cetuximab; EGFR; NK cells; Triple negative breast cancer

Indexed keywords

CD85J ANTIGEN; CETUXIMAB; HLA ANTIGEN; HLA G ANTIGEN; HLA I ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 2; LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN RECEPTOR; LEUKOCYTE ANTIGEN; LILRB1 PROTEIN, HUMAN; MONOCLONAL ANTIBODY;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; BREAST CANCER; CANCER IMMUNOLOGY; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; DISTANT METASTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRIPLE NEGATIVE BREAST CANCER; ADULT; ANTAGONISTS AND INHIBITORS; CASE CONTROL STUDY; FEMALE; IMMUNOLOGY; K562 CELL LINE; METABOLISM; MIDDLE AGED; TRIPLE NEGATIVE BREAST NEOPLASMS; YOUNG ADULT;

ADULT; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, CD; ANTINEOPLASTIC AGENTS; CASE-CONTROL STUDIES; FEMALE; HLA ANTIGENS; HLA-G ANTIGENS; HUMANS; K562 CELLS; KILLER CELLS, NATURAL; MIDDLE AGED; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, IMMUNOLOGIC; TRIPLE NEGATIVE BREAST NEOPLASMS; YOUNG ADULT;

EID: 84929028548     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201445353     Document Type: Article

References (57)

1. Vivier, E., Tomasello, E., Baratin, M., Walzer, T. and Ugolini, S., Functions of natural killer cells. Nat. Immunol. 2008. 9: 503-510.
2. Martin-Fontecha, A., Thomsen, L. L., Brett, S., Gerard, C., Lipp, M., Lanzavecchia, A. and Sallusto, F., Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 2004. 5: 1260-1265.
3. Levy, E. M., Roberti, M. P. and Mordoh, J., Natural killer cells in human cancer: from biological functions to clinical applications. J. Biomed. Biotechnol. 2011. 2011: 676198.
4. Clynes, R. A., Towers, T. L., Presta, L. G. and Ravetch, J. V., Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat. Med. 2000. 6: 443-446.
5. Binyamin, L., Alpaugh, R. K., Hughes, T. L., Lutz, C. T., Campbell, K. S. and Weiner, L. M., Blocking NK cell inhibitory self-recognition promotes antibody-dependent cellular cytotoxicity in a model of anti-lymphoma therapy. J. Immunol. 2008. 180: 6392-6401.
6. Cartron, G., Dacheux, L., Salles, G., Solal-Celigny, P., Bardos, P., Colombat, P. and Watier, H., Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood 2002. 99: 754-758.
7. Weng, W. K. and Levy, R., Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J. Clin. Oncol. 2003. 21: 3940-3947.
8. Beano, A., Signorino, E., Evangelista, A., Brusa, D., Mistrangelo, M., Polimeni, M. A., Spadi, R. et al., Correlation between NK function and response to trastuzumab in metastatic breast cancer patients. J. Transl. Med. 2008. 6: 25.
9. Varchetta, S., Gibelli, N., Oliviero, B., Nardini, E., Gennari, R., Gatti, G., Silva, L. S. et al., Elements related to heterogeneity of antibody-dependent cell cytotoxicity in patients under trastuzumab therapy for primary operable breast cancer overexpressing Her2. Cancer Res. 2007. 67: 11991-11999.
10. Ljunggren, H. G. and Karre, K., Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J. Exp. Med. 1985. 162: 1745-1759.
11. Tassi, I., Klesney-Tait, J. and Colonna, M., Dissecting natural killer cell activation pathways through analysis of genetic mutations in human and mouse. Immunol. Rev. 2006. 214: 92-105.
12. Lanier, L. L., NK cell recognition. Annu. Rev. Immunol. 2005. 23: 225-274.
13. Shiroishi, M., Kuroki, K., Rasubala, L., Tsumoto, K., Kumagai, I., Kurimoto, E., Kato, K. et al., Structural basis for recognition of the nonclassical MHC molecule HLA-G by the leukocyte Ig-like receptor B2 (LILRB2/LIR2/ILT4/CD85d). Proc. Natl. Acad. Sci. USA 2006. 103: 16412-16417.
14. Chapman, T. L., Heikema, A. P., West, A. P., Jr. and Bjorkman, P. J., Crystal structure and ligand binding properties of the D1D2 region of the inhibitory receptor LIR-1 (ILT2). Immunity 2000. 13: 727-736.
15. Vitale, M., Castriconi, R., Parolini, S., Pende, D., Hsu, M. L., Moretta, L., Cosman, D. et al., The leukocyte Ig-like receptor (LIR)-1 for the cytomegalovirus UL18 protein displays a broad specificity for different HLA class I alleles: analysis of LIR-1 + NK cell clones. Int. Immunol. 1999. 11: 29-35.
16. Colonna, M., Navarro, F., Bellon, T., Llano, M., Garcia, P., Samaridis, J., Angman, L. et al., A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med. 1997. 186: 1809-1818.
17. Samaridis, J. and Colonna, M., Cloning of novel immunoglobulin superfamily receptors expressed on human myeloid and lymphoid cells: structural evidence for new stimulatory and inhibitory pathways. Eur. J. Immunol. 1997. 27: 660-665.
18. Navarro, F., Llano, M., Bellon, T., Colonna, M., Geraghty, D. E. and Lopez-Botet, M., The ILT2(LIR1) and CD94/NKG2A NK cell receptors respectively recognize HLA-G1 and HLA-E molecules co-expressed on target cells. Eur. J. Immunol. 1999. 29: 277-283.
19. Cosman, D., Fanger, N., Borges, L., Kubin, M., Chin, W., Peterson, L. and Hsu, M. L., A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 1997. 7: 273-282.
20. Dietrich, J., Cella, M. and Colonna, M., Ig-like transcript 2 (ILT2)/leukocyte Ig-like receptor 1 (LIR1) inhibits TCR signaling and actin cytoskeleton reorganization. J. Immunol. 2001. 166: 2514-2521.
21. Morel, E. and Bellon, T., HLA class I molecules regulate IFN-gamma production induced in NK cells by target cells, viral products, or immature dendritic cells through the inhibitory receptor ILT2/CD85j. J. Immunol. 2008. 181: 2368-2381.
22. Orange, J. S., Formation and function of the lytic NK-cell immunological synapse. Nat. Rev. Immunol. 2008. 8: 713-725.
23. Platonova, S., Cherfils-Vicini, J., Damotte, D., Crozet, L., Vieillard, V., Validire, P., Andre, P. et al., Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res. 2011. 71: 5412-5422.
24. Mamessier, E., Sylvain, A., Thibult, M. L., Houvenaeghel, G., Jacquemier, J., Castellano, R., Goncalves, A. et al., Human breast cancer cells enhance self-tolerance by promoting evasion from NK cell antitumor immunity. J. Clin. Invest. 2011. 121: 3609-3622.
25. Billar, J. A., Dueck, A. C., Stucky, C. C., Gray, R. J., Wasif, N., Northfelt, D. W., McCullough, A. E. et al., Triple-negative breast cancers: unique clinical presentations and outcomes. Ann. Surg. Oncol. 2010. 17 (Suppl 3): 384-390.
26. Carey, L., Winer, E., Viale, G., Cameron, D. and Gianni, L., Triple-negative breast cancer: disease entity or title of convenience? Nat. Rev. Clin. Oncol. 2010. 7: 683-692.
27. vande Rijn, M., Perou, C. M., Tibshirani, R., Haas, P., Kallioniemi, O., Kononen, J., Torhorst, J. et al., Expression of cytokeratins 17 and 5 identifies a group of breast carcinomas with poor clinical outcome. Am. J. Pathol. 2002. 161: 1991-1996.
28. Viale, G., Rotmensz, N., Maisonneuve, P., Bottiglieri, L., Montagna, E., Luini, A., Veronesi, P. et al., Invasive ductal carcinoma of the breast with the "triple-negative" phenotype: prognostic implications of EGFR immunoreactivity. Breast Cancer Res. Treat 2009. 116: 317-328.
29. Ciardiello, F. and Tortora, G., EGFR antagonists in cancer treatment. N. Engl. J. Med. 2008. 358: 1160-1174.
30. Carey, L. A., Rugo, H. S., Marcom, P. K., Mayer, E. L., Esteva, F. J., Ma, C. X., Liu, M. C. et al., TBCRC 001: randomized phase II study of cetuximab in combination with carboplatin in stage IV triple-negative breast cancer. J. Clin. Oncol. 2012. 30: 2615-2623.
31. Baselga, J., Gomez, P., Greil, R., Braga, S., Climent, M. A., Wardley, A. M., Kaufman, B. et al., Randomized phase II study of the anti-epidermal growth factor receptor monoclonal antibody cetuximab with cisplatin versus cisplatin alone in patients with metastatic triple-negative breast cancer. J. Clin. Oncol. 2013. 31: 2586-2592.
32. Roberti, M. P., Rocca, Y. S., Amat, M., Pampena, M. B., Loza, J., Colo, F., Fabiano, V. et al., IL-2- or IL-15-activated NK cells enhance Cetuximab-mediated activity against triple-negative breast cancer in xenografts and in breast cancer patients. Breast Cancer Res. Treat 2012. 136: 659-671.
33. Roberti, M. P., Barrio, M. M., Bravo, A. I., Rocca, Y. S., Arriaga, J. M., Bianchini, M., Mordoh, J. et al., IL-15 and IL-2 increase Cetuximab-mediated cellular cytotoxicity against triple negative breast cancer cell lines expressing EGFR. Breast Cancer Res. Treat 2011. 130: 465-475.
34. LeMaoult, J., Zafaranloo, K., LeDanff, C. and Carosella, E. D., HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen presenting cells, NK cells, and T cells. FASEB J. 2005. 19: 662-664.
35. Wu, J. and Lanier, L. L., Natural killer cells and cancer. Adv. Cancer Res. 2003. 90: 127-156.
36. Zhang, W., Gordon, M., Schultheis, A. M., Yang, D. Y., Nagashima, F., Azuma, M., Chang, H. M. et al., FCGR2A and FCGR3A polymorphisms associated with clinical outcome of epidermal growth factor receptor expressing metastatic colorectal cancer patients treated with single-agent cetuximab. J. Clin. Oncol. 2007. 25: 3712-3718.
37. Musolino, A., Naldi, N., Bortesi, B., Pezzuolo, D., Capelletti, M., Missale, G., Laccabue, D. et al., Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer. J. Clin. Oncol. 2008. 26: 1789-1796.
38. Dewan, M. Z., Terunuma, H., Takada, M., Tanaka, Y., Abe, H., Sata, T., Toi, M. et al., Role of natural killer cells in hormone-independent rapid tumor formation and spontaneous metastasis of breast cancer cells in vivo. Breast Cancer Res. Treat 2007. 104: 267-275.
39. Chretien, A. S., LeRoy, A., Vey, N., Prebet, T., Blaise, D., Fauriat, C. and Olive, D., Cancer-induced alterations of NK-mediated target recognition: current and investigational pharmacological strategies aiming at restoring NK-mediated anti-tumor activity. Front Immunol. 2014. 5: 122.
40. Viel, S., Charrier, E., Marcais, A., Rouzaire, P., Bienvenu, J., Karlin, L., Salles, G. et al., Monitoring NK cell activity in patients with hematological malignancies. Oncoimmunology 2013. 2: e26011.
41. Rocca, Y. S., Roberti, M. P., Arriaga, J. M., Amat, M., Bruno, L., Pampena, M. B., Huertas, E. et al., Altered phenotype in peripheral blood and tumor-associated NK cells from colorectal cancer patients. Innate Immun. 2013. 19: 76-85.
42. Danielou-Lazareth, A., Henry, G., Geromin, D., Khaznadar, Z., Briere, J., Tamouza, R., Cayuela, J. M. et al., At diagnosis, diffuse large B-cell lymphoma patients show impaired rituximab-mediated NK-cell cytotoxicity. Eur. J. Immunol. 2013. 43: 1383-1388.
43. Fregni, G., Messaoudene, M., Fourmentraux-Neves, E., Mazouz-Dorval, S., Chanal, J., Maubec, E., Marinho, E. et al., Phenotypic and functional characteristics of blood natural killer cells from melanoma patients at different clinical stages. PLoS One 2013. 8: e76928.
44. Garner, W. L., Minton, J. P., James, A. G. and Hoffmann, C. C., Human breast cancer and impaired NK cell function. J. Surg. Oncol. 1983. 24: 64-66.
45. Dewan, M. Z., Takada, M., Terunuma, H., Deng, X., Ahmed, S., Yamamoto, N. and Toi, M., Natural killer activity of peripheral-blood mononuclear cells in breast cancer patients. Biomed. Pharmacother. 2009. 63: 703-706.
46. Titus, J. A., Perez, P., Kaubisch, A., Garrido, M. A. and Segal, D. M., Human K/natural killer cells targeted with hetero-cross-linked antibodies specifically lyse tumor cells in vitro and prevent tumor growth in vivo. J. Immunol. 1987. 139: 3153-3158.
47. Lanier, L. L., Ruitenberg, J. J. and Phillips, J. H., Functional and biochemical analysis of CD16 antigen on natural killer cells and granulocytes. J. Immunol. 1988. 141: 3478-3485.
48. Joncker, N. T. and Raulet, D. H., Regulation of NK cell responsiveness to achieve self-tolerance and maximal responses to diseased target cells. Immunol. Rev. 2008. 224: 85-97.
49. Czesnikiewicz-Guzik, M., Lee, W. W., Cui, D., Hiruma, Y., Lamar, D. L., Yang, Z. Z., Ouslander, J. G. et al., T cell subset-specific susceptibility to aging. Clin. Immunol. 2008. 127: 107-118.
50. LeGarff-Tavernier, M., Beziat, V., Decocq, J., Siguret, V., Gandjbakhch, F., Pautas, E., Debre, P. et al., Human NK cells display major phenotypic and functional changes over the life span. Aging Cell 2010. 9: 527-535.
51. Chapman, T. L., Heikeman, A. P. and Bjorkman, P. J., The inhibitory receptor LIR-1 uses a common binding interaction to recognize class I MHC molecules and the viral homolog UL18. Immunity 1999. 11: 603-613.
52. Lepin, E. J., Bastin, J. M., Allan, D. S., Roncador, G., Braud, V. M., Mason, D. Y., vander Merwe, P. A. et al., Functional characterization of HLA-F and binding of HLA-F tetramers to ILT2 and ILT4 receptors. Eur. J. Immunol. 2000. 30: 3552-3561.
53. deKruijf, E. M., vanNes, J. G., Sajet, A., Tummers, Q. R., Putter, H., Osanto, S., Speetjens, F. M. et al., The predictive value of HLA class I tumor cell expression and presence of intratumoral Tregs for chemotherapy in patients with early breast cancer. Clin. Cancer Res. 2010. 16: 1272-1280.
54. Bover, L., Barrio, M., Slavutsky, I., Bravo, A. I., Quintans, C., Bagnati, A., Lema, B. et al., Description of a new human breast cancer cell line, IIB-BR-G, established from a primary undifferentiated tumor. Breast Cancer Res. Treat 1991. 19: 47-56.
55. Neri, S., Mariani, E., Meneghetti, A., Cattini, L. and Facchini, A., Calcein-acetyoxymethyl cytotoxicity assay: standardization of a method allowing additional analyses on recovered effector cells and supernatants. Clin. Diagn. Lab. Immunol. 2001. 8: 1131-1135.
56. Rebmann, V., Lemaoult, J., Rouas-Freiss, N., Carosella, E. D. and Grosse-Wilde, H., Report of the wet workshop for quantification of soluble HLA-G in Essen, 2004. Hum. Immunol. 2005. 66: 853-863.
57. Cabrini, R. L., Brandizzi, D., Schlegel, G., Vidal, S. M. and Santini-Araujo, E., Desarrollo de un dispositivo para realizar microarreglo en un laboratorio convencional. Patología Rev. Latinoam 2011. 49: 239-242.