Fc-Optimized Anti-CD25 Depletes Tumor-Infiltrating Regulatory T Cells and Synergizes with PD-1 Blockade to Eradicate Established Tumors

Immunity

Volumn 46, Issue 4, 2017, Pages 577-586

  Arce Vargas, Frederick ^a,b   Furness, Andrew J S ^a,b,c   Solomon, Isabelle ^a,b   Joshi, Kroopa ^a,b,c   Mekkaoui, Leila ^b   Lesko, Marta H ^a,b   Miranda Rota, Enrique ^b   Dahan, Rony ^d   Georgiou, Andrew ^a,b   Sledzinska, Anna ^a,b   Ben Aissa, Assma ^a,b   Franz, Dafne ^a,b   Werner Sunderland, Mariana ^a,b   Wong, Yien Ning Sophia ^a,b   Henry, Jake Y ^a,b   O'Brien, Tim ^e   Nicol, David ^c   Challacombe, Ben ^e   Beers, Stephen A ^f   Spain, Lavinia ⁱ   Wotherspoon, Andrew ⁱ   Francis, Nicholas ⁱ   Smith, Myles ⁱ   Strauss, Dirk ⁱ   Hayes, Andrew ⁱ   Soultati, Aspasia ⁱ   Stares, Mark ⁱ   Lynch, Joanna ⁱ   Fotiadis, Nicos ⁱ   Fernando, Archana ⁱ   Hazell, Steve ⁱ   Chandra, Ashish ⁱ   Pickering, Lisa ⁱ   Rudman, Sarah ⁱ   Chowdhury, Simon ⁱ   Swanton, Charles ^b,g,i   Jamal Hanjani, Mariam ⁱ   Veeriah, Selvaraju ⁱ   Shafi, Seema ⁱ   Czyzewska Khan, Justyna ⁱ   Johnson, Diana ⁱ   Laycock, Joanne ⁱ   Bosshard Carter, Leticia ⁱ   Goh, Gerald ⁱ   Rosenthal, Rachel ⁱ   Gorman, Pat ⁱ   Murugaesu, Nirupa ⁱ   Hynds, Robert E ⁱ   Wilson, Gareth ⁱ   Birkbak, Nicolai J ⁱ   Watkins, Thomas B K ⁱ   McGranahan, Nicholas ⁱ   Horswell, Stuart ⁱ   Mitter, Richard ⁱ   Escudero, Mickael ⁱ   Stewart, Aengus ⁱ   Van Loo, Peter ⁱ   Rowan, Andrew ⁱ   Xu, Hang ⁱ   Turajlic, Samra ^c,g,i   Hiley, Crispin ⁱ   Abbosh, Christopher ⁱ   Goldman, Jacki ⁱ   Stone, Richard Kevin ⁱ   Denner, Tamara ⁱ   Matthews, Nik ⁱ   Elgar, Greg ⁱ   Ward, Sophia ⁱ   Biggs, Jennifer ⁱ   Costa, Marta ⁱ   Begum, Sharmin ⁱ   Phillimore, Ben ⁱ   Chambers, Tim ⁱ   Nye, Emma ⁱ   Graca, Sofia ⁱ   Al Bakir, Maise ⁱ   Hartley, John A ⁱ   Lowe, Helen L ⁱ   Herrero, Javier ⁱ   Lawrence, David ⁱ   Hayward, Martin ⁱ   Panagiotopoulos, Nikolaos ⁱ   Kolvekar, Shyam ⁱ   Falzon, Mary ⁱ   Borg, Elaine ⁱ   Simeon, Celia ⁱ   Hector, Gemma ⁱ   Smith, Amy ⁱ   Aranda, Marie ⁱ   Novelli, Marco ⁱ   Oukrif, Dahmane ⁱ   Janes, Sam M ⁱ   Thakrar, Ricky ⁱ   Forster, Martin ⁱ   Ahmad, Tanya ⁱ   Lee, Siow Ming ⁱ   Papadatos Pastos, Dionysis ⁱ   Carnell, Dawn ⁱ   Mendes, Ruheena ⁱ   George, Jeremy ⁱ   Navani, Neal ⁱ   Ahmed, Asia ⁱ   Taylor, Magali ⁱ   Choudhary, Junaid ⁱ   Summers, Yvonne ⁱ   Califano, Raffaele ⁱ   Taylor, Paul ⁱ   Shah, Rajesh ⁱ   Krysiak, Piotr ⁱ   Rammohan, Kendadai ⁱ   Fontaine, Eustace ⁱ   Booton, Richard ⁱ   Evison, Matthew ⁱ   Crosbie, Phil ⁱ   Moss, Stuart ⁱ   Idries, Faiza ⁱ   Joseph, Leena ⁱ   Bishop, Paul ⁱ   Chaturved, Anshuman ⁱ   Quinn, Anne Marie ⁱ   Doran, Helen ⁱ   Leek, Angela ⁱ   Harrison, Phil ⁱ   Moore, Katrina ⁱ   Waddington, Rachael ⁱ   Novasio, Juliette ⁱ   Blackhall, Fiona ⁱ   Rogan, Jane ⁱ   Smith, Elaine ⁱ   Dive, Caroline ⁱ   Tugwood, Jonathan ⁱ   Brady, Ged ⁱ   Rothwell, Dominic G ⁱ   Chemi, Francesca ⁱ   Pierce, Jackie ⁱ   Gulati, Sakshi ⁱ   Naidu, Babu ⁱ   Langman, Gerald ⁱ   Trotter, Simon ⁱ   Bellamy, Mary ⁱ   Bancroft, Hollie ⁱ   Kerr, Amy ⁱ   Kadiri, Salma ⁱ   Webb, Joanne ⁱ   Middleton, Gary ⁱ   Djearaman, Madava ⁱ   Fennell, Dean ⁱ   Shaw, Jacqui A ⁱ   Le Quesne, John ⁱ   Moore, David ⁱ   Nakas, Apostolos ⁱ   Rathinam, Sridhar ⁱ   Monteiro, William ⁱ   Marshall, Hilary ⁱ   Nelson, Louise ⁱ   Bennett, Jonathan ⁱ   Riley, Joan ⁱ   Primrose, Lindsay ⁱ   Martinson, Luke ⁱ   Anand, Girija ⁱ   Khan, Sajid ⁱ   Amadi, Anita ⁱ   Nicolson, Marianne ⁱ   Kerr, Keith ⁱ   Palmer, Shirley ⁱ   Remmen, Hardy ⁱ   Miller, Joy ⁱ   Buchan, Keith ⁱ   Chetty, Mahendran ⁱ   Gomersall, Lesley ⁱ   Lester, Jason ⁱ   Edwards, Alison ⁱ   Morgan, Fiona ⁱ   Adams, Haydn ⁱ   Davies, Helen ⁱ   Kornaszewska, Malgorzata ⁱ   Attanoos, Richard ⁱ   Lock, Sara ⁱ   Verjee, Azmina ⁱ   MacKenzie, Mairead ⁱ   Wilcox, Maggie ⁱ   Bell, Harriet ⁱ   Iles, Natasha ⁱ   Hackshaw, Allan ⁱ   Ngai, Yenting ⁱ   Smith, Sean ⁱ   Gower, Nicole ⁱ   Ottensmeier, Christian ⁱ   Chee, Serena ⁱ   Johnson, Benjamin ⁱ   Alzetani, Aiman ⁱ   Shaw, Emily ⁱ   Lim, Eric ⁱ   De Sousa, Paulo ⁱ   Barbosa, Monica Tavares ⁱ   Bowman, Alex ⁱ   Jorda, Simon ⁱ   Rice, Alexandra ⁱ   Raubenheimer, Hilgardt ⁱ   Proli, Chiara ⁱ   Cufari, Maria Elena ⁱ   Ronquillo, John Carlo ⁱ   Kwayie, Angela ⁱ   Bhayani, Harshil ⁱ   Hamilton, Morag ⁱ   Bakar, Yusura ⁱ   Mensah, Natalie ⁱ   Ambrose, Lyn ⁱ   Devaraj, Anand ⁱ   Buderi, Silviu ⁱ   Finch, Jonathan ⁱ   Azcarate, Leire ⁱ   Chavan, Hema ⁱ   Green, Sophie ⁱ   Mashinga, Hillaria ⁱ   Nicholson, Andrew G ⁱ   Lau, Kelvin ⁱ   Sheaff, Michael ⁱ   Schmid, Peter ⁱ   Conibear, John ⁱ   Ezhil, Veni ⁱ   Ismail, Babikir ⁱ   Irvin sellers, Melanie ⁱ   Prakash, Vineet ⁱ   Russell, Peter ⁱ   Light, Teresa ⁱ   Horey, Tracey ⁱ   Danson, Sarah ⁱ   Bury, Jonathan ⁱ   Edwards, John ⁱ   Hill, Jennifer ⁱ   Matthews, Sue ⁱ   Kitsanta, Yota ⁱ   Suvarna, Kim ⁱ   Fisher, Patricia ⁱ   Keerio, Allah Dino ⁱ   Shackcloth, Michael ⁱ   Gosney, John ⁱ   Postmus, Pieter ⁱ   Feeney, Sarah ⁱ   Asante Siaw, Julius ⁱ   Gore, Martin ^c   Larkin, James ^c   Chester, Kerry A ^b   Pule, Martin ^b   Ravetch, Jeffrey V ^d   Marafioti, Teresa ^h   Peggs, Karl S ^a,b   Quezada, Sergio A ^a,b   more..

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^d ROCKEFELLER UNIVERSITY   (United States)

^e GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

^f UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^g THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^h UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

ⁱ NONE

Author keywords

anti CD25; anti PD 1; CD25; Fc gamma receptors; inhibitory Fc receptor; regulatory T cells; Treg depletion; tumor immunotherapy; tumor microenvironment

Indexed keywords

ALPHA CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; CD25 ANTIBODY; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; FC RECEPTOR IIB; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; MONOCLONAL ANTIBODY; NIVOLUMAB; PEMBROLIZUMAB; PROGRAMMED CELL DEATH PROTEIN 1 INHIBITOR; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; FC RECEPTOR; FCGR2B PROTEIN, HUMAN; IMMUNOGLOBULIN FC FRAGMENT; INTERLEUKIN 2 RECEPTOR ALPHA; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN BINDING;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; BLOOD; CANCER GRAFT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLON ADENOCARCINOMA; COLORECTAL CARCINOMA; DISEASE ERADICATION; DRUG POTENTIATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KIDNEY CARCINOMA; LYMPH NODE; LYMPHOCYTE DEPLETION; LYMPHOCYTE PROLIFERATION; MELANOMA; MELANOMA B16; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SARCOMA; T LYMPHOCYTE SUBPOPULATION; TUMOR INFILTRATING REGULATORY T CELL; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; IMMUNOLOGY; IMMUNOTHERAPY; K-562 CELL LINE; KAPLAN MEIER METHOD; METABOLISM; NEOPLASMS; PATHOLOGY; PROCEDURES; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL LINE, TUMOR; FLOW CYTOMETRY; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOTHERAPY; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; K562 CELLS; KAPLAN-MEIER ESTIMATE; LYMPHOCYTE DEPLETION; MICE; NEOPLASMS; PROGRAMMED CELL DEATH 1 RECEPTOR; PROTEIN BINDING; RECEPTORS, IGG; T-LYMPHOCYTES, REGULATORY;

EID: 85017383025     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2017.03.013     Document Type: Article

References (30)

1. Bos, P.D., Plitas, G., Rudra, D., Lee, S.Y., Rudensky, A.Y., Transient regulatory T cell ablation deters oncogene-driven breast cancer and enhances radiotherapy. J. Exp. Med. 210 (2013), 2435–2466.
2. Boyman, O., Sprent, J., The role of interleukin-2 during homeostasis and activation of the immune system. Nat. Rev. Immunol. 12 (2012), 180–190.
3. Bulliard, Y., Jolicoeur, R., Zhang, J., Dranoff, G., Wilson, N.S., Brogdon, J.L., OX40 engagement depletes intratumoral Tregs via activating FcγRs, leading to antitumor efficacy. Immunol. Cell Biol. 92 (2014), 475–480.
4. Clynes, R.A., Towers, T.L., Presta, L.G., Ravetch, J.V., Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat. Med. 6 (2000), 443–446.
5. Coe, D., Begom, S., Addey, C., White, M., Dyson, J., Chai, J.G., Depletion of regulatory T cells by anti-GITR mAb as a novel mechanism for cancer immunotherapy. Cancer Immunol. Immunother. 59 (2010), 1367–1377.
6. Dahan, R., Sega, E., Engelhardt, J., Selby, M., Korman, A.J., Ravetch, J.V., FcγRs modulate the anti-tumor activity of antibodies targeting the PD-1/PD-L1 axis. Cancer Cell 28 (2015), 285–295.
7. Dannull, J., Su, Z., Rizzieri, D., Yang, B.K., Coleman, D., Yancey, D., Zhang, A., Dahm, P., Chao, N., Gilboa, E., Vieweg, J., Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J. Clin. Invest. 115 (2005), 3623–3633.
8. Elpek, K.G., Lacelle, C., Singh, N.P., Yolcu, E.S., Shirwan, H., CD4+CD25+ T regulatory cells dominate multiple immune evasion mechanisms in early but not late phases of tumor development in a B cell lymphoma model. J. Immunol. 178 (2007), 6840–6848.
9. Goding, S.R., Wilson, K.A., Xie, Y., Harris, K.M., Baxi, A., Akpinarli, A., Fulton, A., Tamada, K., Strome, S.E., Antony, P.A., Restoring immune function of tumor-specific CD4+ T cells during recurrence of melanoma. J. Immunol. 190 (2013), 4899–4909.
10. Golgher, D., Jones, E., Powrie, F., Elliott, T., Gallimore, A., Depletion of CD25+ regulatory cells uncovers immune responses to shared murine tumor rejection antigens. Eur. J. Immunol. 32 (2002), 3267–3275.
11. Hodi, F.S., Butler, M., Oble, D.A., Seiden, M.V., Haluska, F.G., Kruse, A., Macrae, S., Nelson, M., Canning, C., Lowy, I., et al. Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients. Proc. Natl. Acad. Sci. USA 105 (2008), 3005–3010.
12. Jacobs, J.F.M., Punt, C.J.A., Lesterhuis, W.J., Sutmuller, R.P.M., Brouwer, H.M.-L.H., Scharenborg, N.M., Klasen, I.S., Hilbrands, L.B., Figdor, C.G., de Vries, I.J.M., Adema, G.J., Dendritic cell vaccination in combination with anti-CD25 monoclonal antibody treatment: a phase I/II study in metastatic melanoma patients. Clin. Cancer Res. 16 (2010), 5067–5078.
13. Jones, E., Dahm-Vicker, M., Simon, A.K., Green, A., Powrie, F., Cerundolo, V., Gallimore, A., Depletion of CD25+ regulatory cells results in suppression of melanoma growth and induction of autoreactivity in mice. Cancer Immun., 2, 2002, 1.
14. Larkin, J., Chiarion-Sileni, V., Gonzalez, R., Grob, J.J., Cowey, C.L., Lao, C.D., Schadendorf, D., Dummer, R., Smylie, M., Rutkowski, P., et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N. Engl. J. Med. 373 (2015), 23–34.
15. Luke, J.J., Zha, Y., Matijevich, K., Gajewski, T.F., Single dose denileukin diftitox does not enhance vaccine-induced T cell responses or effectively deplete Tregs in advanced melanoma: immune monitoring and clinical results of a randomized phase II trial. J. Immunother. Cancer, 4, 2016, 35.
16. Nimmerjahn, F., Ravetch, J.V., Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 310 (2005), 1510–1512.
17. Onizuka, S., Tawara, I., Shimizu, J., Sakaguchi, S., Fujita, T., Nakayama, E., Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res. 59 (1999), 3128–3133.
18. Peggs, K.S., Quezada, S.A., Chambers, C.A., Korman, A.J., Allison, J.P., Blockade of CTLA-4 on both effector and regulatory T cell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. J. Exp. Med. 206 (2009), 1717–1725.
19. Quezada, S.A., Peggs, K.S., Curran, M.A., Allison, J.P., CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J. Clin. Invest. 116 (2006), 1935–1945.
20. Quezada, S.A., Peggs, K.S., Simpson, T.R., Shen, Y., Littman, D.R., Allison, J.P., Limited tumor infiltration by activated T effector cells restricts the therapeutic activity of regulatory T cell depletion against established melanoma. J. Exp. Med. 205 (2008), 2125–2138.
21. Rech, A.J., Mick, R., Martin, S., Recio, A., Aqui, N.A., Powell, D.J. Jr., Colligon, T.A., Trosko, J.A., Leinbach, L.I., Pletcher, C.H., et al. CD25 blockade depletes and selectively reprograms regulatory T cells in concert with immunotherapy in cancer patients. Sci. Transl. Med., 4, 2012, 134ra62.
22. Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M., Toda, M., Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155 (1995), 1151–1164.
23. Selby, M.J., Engelhardt, J.J., Quigley, M., Henning, K.A., Chen, T., Srinivasan, M., Korman, A.J., Anti-CTLA-4 antibodies of IgG2a isotype enhance antitumor activity through reduction of intratumoral regulatory T cells. Cancer Immunol. Res. 1 (2013), 32–42.
24. Setiady, Y.Y., Coccia, J.A., Park, P.U., In vivo depletion of CD4+FOXP3+ Treg cells by the PC61 anti-CD25 monoclonal antibody is mediated by FcgammaRIII+ phagocytes. Eur. J. Immunol. 40 (2010), 780–786.
25. Shang, B., Liu, Y., Jiang, S.J., Liu, Y., Prognostic value of tumor-infiltrating FoxP3+ regulatory T cells in cancers: a systematic review and meta-analysis. Sci. Rep., 5, 2015, 15179.
26. Shimizu, J., Yamazaki, S., Sakaguchi, S., Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity. J. Immunol. 163 (1999), 5211–5218.
27. Simpson, T.R., Li, F., Montalvo-Ortiz, W., Sepulveda, M.A., Bergerhoff, K., Arce, F., Roddie, C., Henry, J.Y., Yagita, H., Wolchok, J.D., et al. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. J. Exp. Med. 210 (2013), 1695–1710.
28. Sutmuller, R.P., van Duivenvoorde, L.M., van Elsas, A., Schumacher, T.N., Wildenberg, M.E., Allison, J.P., Toes, R.E., Offringa, R., Melief, C.J., Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J. Exp. Med. 194 (2001), 823–832.
29. 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.
30. van Elsas, A., Sutmuller, R.P., Hurwitz, A.A., Ziskin, J., Villasenor, J., Medema, J.P., Overwijk, W.W., Restifo, N.P., Melief, C.J., Offringa, R., Allison, J.P., Elucidating the autoimmune and antitumor effector mechanisms of a treatment based on cytotoxic T lymphocyte antigen-4 blockade in combination with a B16 melanoma vaccine: comparison of prophylaxis and therapy. J. Exp. Med. 194 (2001), 481–489.