Neutrophils Kill Antibody-Opsonized Cancer Cells by Trogoptosis

Cell Reports

Volumn 23, Issue 13, 2018, Pages 3946-3959.e6

  Matlung, Hanke L ^a   Babes, Liane ^b   Zhao, Xi Wen ^a   van Houdt, Michel ^a   Treffers, Louise W ^a   van Rees, Dieke J ^a   Franke, Katka ^a   Schornagel, Karin ^a   Verkuijlen, Paul ^a   Janssen, Hans ^c   Halonen, Pasi ^c   Lieftink, Cor ^c   Beijersbergen, Roderick L ^c   Leusen, Jeanette H W ^d   Boelens, Jaap J ^d   Kuhnle, Ingrid ^e   van der Werff Ten Bosch, Jutte ^f   Seeger, Karl ^g   Rutella, Sergio ^h   Pagliara, Daria ⁱ   Matozaki, Takashi ^j   Suzuki, Eiji ^k   Menke van der Houven van Oordt, Catharina Willemien ^l   van Bruggen, Robin ^a   Roos, Dirk ^a   van Lier, Rene A W ^a   Kuijpers, Taco W ^a   Kubes, Paul ^b   van den Berg, Timo K ^a,l   more..

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF CALGARY   (Canada)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^e UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^f UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

^g CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^h SIDRA MEDICAL AND RESEARCH CENTER   (Qatar)

ⁱ BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^j KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^k KYOTO UNIVERSITY HOSPITAL   (Japan)

^l VU UNIVERSITY MEDICAL CENTER   (Netherlands)

more..

Author keywords

antibody dependent cellular cytotoxicity; CD47 SIRP interaction; neutrophils; trogocytosis; trogoptosis

Indexed keywords

CD11B ANTIGEN; CD18 ANTIGEN; CD47 ANTIGEN; MEMBRANE RECEPTOR; SIGNAL REGULATORY PROTEIN ALPHA; UNCLASSIFIED DRUG; FC RECEPTOR; IMMUNOGLOBULIN RECEPTOR; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CANCER CELL; CELL DAMAGE; CELL DEATH; CELL MEMBRANE; CONJUGATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NEUTROPHIL; NONHUMAN; OPSONIZATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TROGOPTOSIS; ALLOTRANSPLANTATION; ANIMAL; C57BL MOUSE; EXPERIMENTAL MELANOMA; GENETICS; IMMUNOLOGY; METABOLISM; NEOPLASM; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; CD11B ANTIGEN; CD18 ANTIGENS; CD47 ANTIGEN; CELL LINE, TUMOR; FEMALE; HUMANS; MALE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; NEOPLASMS; NEUTROPHILS; RECEPTORS, IGG; RECEPTORS, IMMUNOLOGIC; TRANSPLANTATION, HOMOLOGOUS;

EID: 85048859204     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2018.05.082     Document Type: Article

References (69)

1. Ahrens, S., Zelenay, S., Sancho, D., Hanč, P., Kjær, S., Feest, C., Fletcher, G., Durkin, C., Postigo, A., Skehel, M., et al. F-actin is an evolutionarily conserved damage-associated molecular pattern recognized by DNGR-1, a receptor for dead cells. Immunity 36 (2012), 635–645.
2. Albanesi, M., Mancardi, D.A., Jönsson, F., Iannascoli, B., Fiette, L., Di Santo, J.P., Lowell, C.A., Bruhns, P., Neutrophils mediate antibody-induced antitumor effects in mice. Blood 122 (2013), 3160–3164.
3. Barclay, A.N., van den Berg, T.K., The Interaction Between Signal Regulatory Protein Alpha (SIRPalpha) and CD47: Structure, Function, and Therapeutic Target. Annu. Rev. Immunol. 32 (2014), 25–50.
4. Borregaard, N., Sørensen, O.E., Theilgaard-Mönch, K., Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 28 (2007), 340–345.
5. Bryceson, Y.T., Long, E.O., Line of attack: NK cell specificity and integration of signals. Curr. Opin. Immunol. 20 (2008), 344–352.
6. Calafat, J., Janssen, H., Ståhle-Bäckdahl, M., Zuurbier, A.E., Knol, E.F., Egesten, A., Human monocytes and neutrophils store transforming growth factor-alpha in a subpopulation of cytoplasmic granules. Blood 90 (1997), 1255–1266.
7. Chao, M.P., Alizadeh, A.A., Tang, C., Myklebust, J.H., Varghese, B., Gill, S., Jan, M., Cha, A.C., Chan, C.K., Tan, B.T., et al. Anti-CD47 antibody synergizes with rituximab to promote phagocytosis and eradicate non-Hodgkin lymphoma. Cell 142 (2010), 699–713.
8. Chao, M.P., Jaiswal, S., Weissman-Tsukamoto, R., Alizadeh, A.A., Gentles, A.J., Volkmer, J., Weiskopf, K., Willingham, S.B., Raveh, T., Park, C.Y., et al. Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Sci. Transl. Med., 2, 2010, 63ra94.
9. Chen, G.Y., Nuñez, G., Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 10 (2010), 826–837.
10. de Saint Basile, G., Ménasché, G., Fischer, A., Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules. Nat. Rev. Immunol. 10 (2010), 568–579.
11. DiLillo, D.J., Ravetch, J.V., Differential Fc-Receptor Engagement Drives an Anti-tumor Vaccinal Effect. Cell 161 (2015), 1035–1045.
12. Dustin, M.L., Long, E.O., Cytotoxic immunological synapses. Immunol. Rev. 235 (2010), 24–34.
13. Eruslanov, E.B., Bhojnagarwala, P.S., Quatromoni, J.G., Stephen, T.L., Ranganathan, A., Deshpande, C., Akimova, T., Vachani, A., Litzky, L., Hancock, W.W., et al. Tumor-associated neutrophils stimulate T cell responses in early-stage human lung cancer. J. Clin. Invest. 124 (2014), 5466–5480.
14. Fevre, C., Bestebroer, J., Mebius, M.M., de Haas, C.J., van Strijp, J.A., Fitzgerald, J.R., Haas, P.J., Staphylococcus aureus proteins SSL6 and SElX interact with neutrophil receptors as identified using secretome phage display. Cell. Microbiol. 16 (2014), 1646–1665.
15. Glennie, M.J., van de Winkel, J.G., Renaissance of cancer therapeutic antibodies. Drug Discov. Today 8 (2003), 503–510.
16. Gül, N., Babes, L., Siegmund, K., Korthouwer, R., Bögels, M., Braster, R., Vidarsson, G., ten Hagen, T.L., Kubes, P., van Egmond, M., Macrophages eliminate circulating tumor cells after monoclonal antibody therapy. J. Clin. Invest. 124 (2014), 812–823.
17. Hawkins, P.T., Stephens, L.R., Suire, S., Wilson, M., PI3K signaling in neutrophils. Curr. Top. Microbiol. Immunol. 346 (2010), 183–202.
18. Hernandez-Ilizaliturri, F.J., Jupudy, V., Ostberg, J., Oflazoglu, E., Huberman, A., Repasky, E., Czuczman, M.S., Neutrophils contribute to the biological antitumor activity of rituximab in a non-Hodgkin's lymphoma severe combined immunodeficiency mouse model. Clin. Cancer Res. 9 (2003), 5866–5873.
19. Herrero-Turrión, M.J., Calafat, J., Janssen, H., Fukuda, M., Mollinedo, F., Rab27a regulates exocytosis of tertiary and specific granules in human neutrophils. J. Immunol. 181 (2008), 3793–3803.
20. Inagaki, K., Yamao, T., Noguchi, T., Matozaki, T., Fukunaga, K., Takada, T., Hosooka, T., Akira, S., Kasuga, M., SHPS-1 regulates integrin-mediated cytoskeletal reorganization and cell motility. EMBO J. 19 (2000), 6721–6731.
21. Jaiswal, S., Jamieson, C.H., Pang, W.W., Park, C.Y., Chao, M.P., Majeti, R., Traver, D., van Rooijen, N., Weissman, I.L., CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 138 (2009), 271–285.
22. Joly, E., Hudrisier, D., What is trogocytosis and what is its purpose?. Nat. Immunol., 4, 2003, 815.
23. Kuijpers, K.C., Kuijpers, T.W., Zeijlemaker, W.P., Lucas, C.J., van Lier, R.A., Miedema, F., Analysis of the role of leukocyte function-associated antigen-1 in activation of human influenza virus-specific T cell clones. J. Immunol. 144 (1990), 3281–3287.
24. Kuijpers, T.W., Tool, A.T., van der Schoot, C.E., Ginsel, L.A., Onderwater, J.J., Roos, D., Verhoeven, A.J., Membrane surface antigen expression on neutrophils: a reappraisal of the use of surface markers for neutrophil activation. Blood 78 (1991), 1105–1111.
25. Liu, X., Pu, Y., Cron, K., Deng, L., Kline, J., Frazier, W.A., Xu, H., Peng, H., Fu, Y.X., Xu, M.M., CD47 blockade triggers T cell-mediated destruction of immunogenic tumors. Nat. Med. 21 (2015), 1209–1215.
26. Majeti, R., Chao, M.P., Alizadeh, A.A., Pang, W.W., Jaiswal, S., Gibbs, K.D. Jr., van Rooijen, N., Weissman, I.L., CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 138 (2009), 286–299.
27. Martínez-Martín, N., Fernández-Arenas, E., Cemerski, S., Delgado, P., Turner, M., Heuser, J., Irvine, D.J., Huang, B., Bustelo, X.R., Shaw, A., Alarcón, B., T cell receptor internalization from the immunological synapse is mediated by TC21 and RhoG GTPase-dependent phagocytosis. Immunity 35 (2011), 208–222.
28. Matzinger, P., The danger model: a renewed sense of self. Science 296 (2002), 301–305.
29. Meeths, M., Entesarian, M., Al-Herz, W., Chiang, S.C., Wood, S.M., Al-Ateeqi, W., Almazan, F., Boelens, J.J., Hasle, H., Ifversen, M., et al. Spectrum of clinical presentations in familial hemophagocytic lymphohistiocytosis type 5 patients with mutations in STXBP2. Blood 116 (2010), 2635–2643.
30. Mócsai, A., Ruland, J., Tybulewicz, V.L., The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat. Rev. Immunol. 10 (2010), 387–402.
31. Montalvao, F., Garcia, Z., Celli, S., Breart, B., Deguine, J., Van Rooijen, N., Bousso, P., The mechanism of anti-CD20-mediated B cell depletion revealed by intravital imaging. J. Clin. Invest. 123 (2013), 5098–5103.
32. Musolino, A., Naldi, N., Bortesi, B., Pezzuolo, D., Capelletti, M., Missale, G., Laccabue, D., Zerbini, A., Camisa, R., Bisagni, G., 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. 26 (2008), 1789–1796.
33. Nimmerjahn, F., Ravetch, J.V., Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 8 (2008), 34–47.
34. Nimmerjahn, F., Gordan, S., Lux, A., FcγR dependent mechanisms of cytotoxic, agonistic, and neutralizing antibody activities. Trends Immunol. 36 (2015), 325–336.
35. Oldham, R.K., Dillman, R.O., Monoclonal antibodies in cancer therapy: 25 years of progress. J. Clin. Oncol. 26 (2008), 1774–1777.
36. Ralston, K.S., Solga, M.D., Mackey-Lawrence, N.M., Somlata, Bhattacharya, A., Petri, W.A. Jr., Trogocytosis by Entamoeba histolytica contributes to cell killing and tissue invasion. Nature 508 (2014), 526–530.
37. Reeves, E.P., Lu, H., Jacobs, H.L., Messina, C.G., Bolsover, S., Gabella, G., Potma, E.O., Warley, A., Roes, J., Segal, A.W., Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416 (2002), 291–297.
38. Ring, N.G., Herndler-Brandstetter, D., Weiskopf, K., Shan, L., Volkmer, J.P., George, B.M., Lietzenmayer, M., McKenna, K.M., Naik, T.J., McCarty, A., et al. Anti-SIRPα antibody immunotherapy enhances neutrophil and macrophage antitumor activity. Proc. Natl. Acad. Sci. USA 114 (2017), E10578–E10585.
39. Roos, D., van Bruggen, R., Meischl, C., Oxidative killing of microbes by neutrophils. Microbes Infect. 5 (2003), 1307–1315.
40. Rosseau, S., Selhorst, J., Wiechmann, K., Leissner, K., Maus, U., Mayer, K., Grimminger, F., Seeger, W., Lohmeyer, J., Monocyte migration through the alveolar epithelial barrier: adhesion molecule mechanisms and impact of chemokines. J. Immunol. 164 (2000), 427–435.
41. Sancho, D., Mourão-Sá, D., Joffre, O.P., Schulz, O., Rogers, N.C., Pennington, D.J., Carlyle, J.R., Reis e Sousa, C., Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J. Clin. Invest. 118 (2008), 2098–2110.
42. Segal, A.W., How neutrophils kill microbes. Annu. Rev. Immunol. 23 (2005), 197–223.
43. Siders, W.M., Shields, J., Garron, C., Hu, Y., Boutin, P., Shankara, S., Weber, W., Roberts, B., Kaplan, J.M., Involvement of neutrophils and natural killer cells in the anti-tumor activity of alemtuzumab in xenograft tumor models. Leuk. Lymphoma 51 (2010), 1293–1304.
44. Somlata, N.-T., Nakada-Tsukui, K., Nozaki, T., AGC family kinase 1 participates in trogocytosis but not in phagocytosis in Entamoeba histolytica. Nat. Commun., 8, 2017, 101.
45. Soto-Pantoja, D.R., Miller, T.W., Frazier, W.A., Roberts, D.D., Inhibitory signaling through signal regulatory protein-α is not sufficient to explain the antitumor activities of CD47 antibodies. Proc. Natl. Acad. Sci. USA 109 (2012), E2842–E2845 author reply E2844–E2845.
46. Soto-Pantoja, D.R., Terabe, M., Ghosh, A., Ridnour, L.A., DeGraff, W.G., Wink, D.A., Berzofsky, J.A., Roberts, D.D., CD47 in the tumor microenvironment limits cooperation between antitumor T-cell immunity and radiotherapy. Cancer Res. 74 (2014), 6771–6783.
47. Strome, S.E., Sausville, E.A., Mann, D., A mechanistic perspective of monoclonal antibodies in cancer therapy beyond target-related effects. Oncologist 12 (2007), 1084–1095.
48. Suzuki, E., Kataoka, T.R., Hirata, M., Kawaguchi, K., Nishie, M., Haga, H., Toi, M., Trogocytosis-mediated expression of HER2 on immune cells may be associated with a pathological complete response to trastuzumab-based primary systemic therapy in HER2-overexpressing breast cancer patients. BMC Cancer, 15, 2015, 39.
49. Tabiasco, J., Espinosa, E., Hudrisier, D., Joly, E., Fournié, J.J., Vercellone, A., Active trans-synaptic capture of membrane fragments by natural killer cells. Eur. J. Immunol. 32 (2002), 1502–1508.
50. Taylor, R.P., Lindorfer, M.A., Fcγ-receptor-mediated trogocytosis impacts mAb-based therapies: historical precedence and recent developments. Blood 125 (2015), 762–766.
51. Tintinger, G., Steel, H.C., Anderson, R., Taming the neutrophil: calcium clearance and influx mechanisms as novel targets for pharmacological control. Clin. Exp. Immunol. 141 (2005), 191–200.
52. Topalian, S.L., Drake, C.G., Pardoll, D.M., Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell 27 (2015), 450–461.
53. Treffers, L.W., Zhao, X.W., van der Heijden, J., Nagelkerke, S.Q., van Rees, D.J., Gonzalez, P., Geissler, J., Verkuijlen, P., van Houdt, M., de Boer, M., et al. Genetic variation of human neutrophil Fcγ receptors and SIRPα in antibody-dependent cellular cytotoxicity towards cancer cells. Eur. J. Immunol. 48 (2018), 344–354.
54. Tseng, D., Volkmer, J.P., Willingham, S.B., Contreras-Trujillo, H., Fathman, J.W., Fernhoff, N.B., Seita, J., Inlay, M.A., Weiskopf, K., Miyanishi, M., Weissman, I.L., Anti-CD47 antibody-mediated phagocytosis of cancer by macrophages primes an effective antitumor T-cell response. Proc. Natl. Acad. Sci. USA 110 (2013), 11103–11108.
55. Valgardsdottir, R., Cattaneo, I., Klein, C., Introna, M., Figliuzzi, M., Golay, J., Human neutrophils mediate trogocytosis rather than phagocytosis of CLL B cells opsonized with anti-CD20 antibodies. Blood 129 (2017), 2636–2644.
56. van Beek, E.M., Zarate, J.A., van Bruggen, R., Schornagel, K., Tool, A.T., Matozaki, T., Kraal, G., Roos, D., van den Berg, T.K., SIRPα controls the activity of the phagocyte NADPH oxidase by restricting the expression of gp91(phox). Cell Rep. 2 (2012), 748–755.
57. van Egmond, M., Bakema, J.E., Neutrophils as effector cells for antibody-based immunotherapy of cancer. Semin. Cancer Biol. 23 (2013), 190–199.
58. van de Vijver, E., Maddalena, A., Sanal, Ö., Holland, S.M., Uzel, G., Madkaikar, M., de Boer, M., van Leeuwen, K., Köker, M.Y., Parvaneh, N., et al. Hematologically important mutations: leukocyte adhesion deficiency (first update). Blood Cells Mol. Dis. 48 (2012), 53–61.
59. van den Berg, T.K., van Bruggen, R., Loss of CD47 makes dendritic cells see red. Immunity 43 (2015), 622–624.
60. van Spriel, A.B., Leusen, J.H., van Egmond, M., Dijkman, H.B., Assmann, K.J., Mayadas, T.N., van de Winkel, J.G., Mac-1 (CD11b/CD18) is essential for Fc receptor-mediated neutrophil cytotoxicity and immunologic synapse formation. Blood 97 (2001), 2478–2486.
61. van Spriel, A.B., van Ojik, H.H., Bakker, A., Jansen, M.J., van de Winkel, J.G., Mac-1 (CD11b/CD18) is crucial for effective Fc receptor-mediated immunity to melanoma. Blood 101 (2003), 253–258.
62. Velmurugan, R., Challa, D.K., Ram, S., Ober, R.J., Ward, E.S., Macrophage-Mediated Trogocytosis Leads to Death of Antibody-Opsonized Tumor Cells. Mol. Cancer Ther. 15 (2016), 1879–1889.
63. Weiskopf, K., Ring, A.M., Ho, C.C., Volkmer, J.P., Levin, A.M., Volkmer, A.K., Ozkan, E., Fernhoff, N.B., van de Rijn, M., Weissman, I.L., Garcia, K.C., Engineered SIRPα variants as immunotherapeutic adjuvants to anticancer antibodies. Science 341 (2013), 88–91.
64. Yi, T., Li, J., Chen, H., Wu, J., An, J., Xu, Y., Hu, Y., Lowell, C.A., Cyster, J.G., Splenic Dendritic Cells Survey Red Blood Cells for Missing Self-CD47 to Trigger Adaptive Immune Responses. Immunity 43 (2015), 764–775.
65. Zhao, X.W., van Beek, E.M., Schornagel, K., van der Maaden, H., van Houdt, M., Otten, M.A., Finetti, P., van Egmond, M., Matozaki, T., Kraal, G., et al. CD47-signal regulatory protein-α (SIRPα) interactions form a barrier for antibody-mediated tumor cell destruction. Proc. Natl. Acad. Sci. USA 108 (2011), 18342–18347.
66. Zhao, X.W., Kuijpers, T.W., van den Berg, T.K., Is targeting of CD47-SIRPα enough for treating hematopoietic malignancy?. Blood 119 (2012), 4333–4334 author reply 4334–4335.
67. Zhao, X.W., Matlung, H.L., Kuijpers, T.W., van den Berg, T.K., On the mechanism of CD47 targeting in cancer. Proc. Natl. Acad. Sci. USA, 109, 2012, E2843 author reply E2844–E2845.
68. Zhao, X.W., Gazendam, R.P., Drewniak, A., van Houdt, M., Tool, A.T., van Hamme, J.L., Kustiawan, I., Meijer, A.B., Janssen, H., Russell, D.G., et al. Defects in neutrophil granule mobilization and bactericidal activity in familial hemophagocytic lymphohistiocytosis type 5 (FHL-5) syndrome caused by STXBP2/Munc18-2 mutations. Blood 122 (2013), 109–111.
69. Zhu, E.F., Gai, S.A., Opel, C.F., Kwan, B.H., Surana, R., Mihm, M.C., Kauke, M.J., Moynihan, K.D., Angelini, A., Williams, R.T., et al. Synergistic innate and adaptive immune response to combination immunotherapy with anti-tumor antigen antibodies and extended serum half-life IL-2. Cancer Cell 27 (2015), 489–501.