Advanced search
Publication Cover
mAbs Volume 15, 2023 - Issue 1
Submit an article Journal homepage
3,391
Views
0
CrossRef citations to date
0
Altmetric
Report

Generation of a novel fully human non-superagonistic anti-CD28 antibody with efficient and safe T-cell co-stimulation properties

Abdullah Elsayeda Philochem AG, Libernstrasse 3, Otelfingen, Switzerland;b Department of Chemistry and Applied Biosciences, Swiss Federal Institute of Technology (ETH Zürich), Zurich, SwitzerlandORCID Iconhttps://orcid.org/0000-0001-7080-0853View further author information
ORCID Icon,
Christian Pellegrinoc Department of Medical Oncology and Hematology, University Hospital Zurich and University of Zurich, Zurich, SwitzerlandORCID Iconhttps://orcid.org/0000-0001-7898-9988View further author information
ORCID Icon,
Louis Plüssa Philochem AG, Libernstrasse 3, Otelfingen, Switzerland;b Department of Chemistry and Applied Biosciences, Swiss Federal Institute of Technology (ETH Zürich), Zurich, SwitzerlandView further author information
,
Frederik Peisserta Philochem AG, Libernstrasse 3, Otelfingen, SwitzerlandView further author information
,
Ramon Benzb Department of Chemistry and Applied Biosciences, Swiss Federal Institute of Technology (ETH Zürich), Zurich, SwitzerlandView further author information
,
Franziska Ulrichb Department of Chemistry and Applied Biosciences, Swiss Federal Institute of Technology (ETH Zürich), Zurich, SwitzerlandView further author information
,
Gudrun Thorhallsdottira Philochem AG, Libernstrasse 3, Otelfingen, Switzerland;b Department of Chemistry and Applied Biosciences, Swiss Federal Institute of Technology (ETH Zürich), Zurich, SwitzerlandORCID Iconhttps://orcid.org/0009-0005-0604-7728View further author information
ORCID Icon,
Sheila Dakhel Plazaa Philochem AG, Libernstrasse 3, Otelfingen, SwitzerlandView further author information
,
Alessandra Villaa Philochem AG, Libernstrasse 3, Otelfingen, SwitzerlandView further author information
,
Jacqueline Mocka Philochem AG, Libernstrasse 3, Otelfingen, SwitzerlandORCID Iconhttps://orcid.org/0000-0002-4618-1113View further author information
ORCID Icon,
Emanuele Pucaa Philochem AG, Libernstrasse 3, Otelfingen, SwitzerlandORCID Iconhttps://orcid.org/0000-0002-2869-3203View further author information
ORCID Icon,
Roberto De Lucaa Philochem AG, Libernstrasse 3, Otelfingen, SwitzerlandORCID Iconhttps://orcid.org/0000-0001-7519-8689View further author information
ORCID Icon,
Markus G. Manzc Department of Medical Oncology and Hematology, University Hospital Zurich and University of Zurich, Zurich, SwitzerlandORCID Iconhttps://orcid.org/0000-0002-4676-7931View further author information
ORCID Icon,
Cornelia Halinb Department of Chemistry and Applied Biosciences, Swiss Federal Institute of Technology (ETH Zürich), Zurich, SwitzerlandORCID Iconhttps://orcid.org/0000-0002-7899-2850View further author information
ORCID Icon &
Dario Neria Philochem AG, Libernstrasse 3, Otelfingen, Switzerland;b Department of Chemistry and Applied Biosciences, Swiss Federal Institute of Technology (ETH Zürich), Zurich, Switzerland;d Philogen SpA, Siena (S), ItalyCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0001-5234-7370View further author information
ORCID Icon show all
Article: 2220839 | Received 17 Feb 2023, Accepted 30 May 2023, Published online: 08 Jun 2023

References

  • Allison JP, McIntyre BW, Bloch D. Tumor-specific antigen of murine T-lymphoma defined with monoclonal antibody. J Immunol. 1982;129(5):2293–12. PMID: 6181166. doi:10.4049/jimmunol.129.5.2293.
  • Hedrick SM, Cohen DI, Nielsen EA, Davis MM. Isolation of cDNA clones encoding T cell-specific membrane-associated proteins. Nature. 1984;308:149–53. doi:10.1038/308149a0. PMID: 6199676.
  • Yanagi Y, Yoshikai Y, Leggett K, Clark SP, Aleksander I, Mak TW. A human T cell-specific cDNA clone encodes a protein having extensive homology to immunoglobulin chains. Nature. 1984;308:145–49. doi:10.1038/308145a0. PMID: 6336315.
  • Davis MM, Bjorkman PJ. T-cell antigen receptor genes and T-cell recognition. Nature. 1988;334:395–402. doi:10.1038/334395a0. PMID: 3043226.
  • La Gruta NL, Gras S, Daley SR, Thomas PG, Rossjohn J. Understanding the drivers of MHC restriction of T cell receptors. Nat Rev Immunol. 2018;18:467–78. doi:10.1038/s41577-018-0007-5. PMID: 29636542.
  • Weiss A, Stobo JD. Requirement for the coexpression of T3 and the T cell antigen receptor on a malignant human T cell line. J Exp Med. 1984;160:1284–99. doi:10.1084/jem.160.5.1284. PMID: 6208306.
  • Ohashi PS, Mak TW, Van den Elsen P, Yanagi Y, Yoshikai Y, Calman AF, Terhorst C, Stobo JD, Weiss A. Reconstitution of an active surface T3/T-cell antigen receptor by DNA transfer. Nature. 1985;316:606–09. doi:10.1038/316606a0. PMID: 4033759.
  • Weiss A, Imboden J, Hardy K, Manger B, Terhorst C, Stobo J. The role of the T3/antigen receptor complex in T-cell activation. Annu Rev Immunol. 1986;4:593–619. doi:10.1146/annurev.iy.04.040186.003113. PMID: 2939858.
  • Janeway CA Jr. T-cell development. Accessories or coreceptors? Nature. 1988;335:208–10. PMID: 3261842. doi:10.1038/335208a0.
  • Mueller DL, Jenkins MK, Schwartz RH. Clonal expansion versus functional clonal inactivation: a costimulatory signalling pathway determines the outcome of T cell antigen receptor occupancy. Annu Rev Immunol. 1989;7:445–80. doi:10.1146/annurev.iy.07.040189.002305. PMID: 2653373.
  • Appleman LJ, Boussiotis VA. T cell anergy and costimulation. Immunol Rev. 2003;192:161–80. doi:10.1034/j.1600-065x.2003.00009.x. PMID: 12670403.
  • Jenkins MK, Taylor PS, Norton SD, Urdahl KB. CD28 delivers a costimulatory signal involved in antigen-specific IL-2 production by human T cells. J Immunol. 1991;147(8):2461–66. PMID: 1717561. doi:10.4049/jimmunol.147.8.2461.
  • June CH, Ledbetter JA, Gillespie MM, Lindsten T, Thompson CB. T-cell proliferation involving the CD28 pathway is associated with cyclosporine-resistant interleukin 2 gene expression. Mol Cell Biol. 1987;7(12):4472–81. PMID: 2830495. doi:10.1128/mcb.7.12.4472-4481.1987.
  • Martin PJ, Ledbetter JA, Morishita Y, June CH, Beatty PG, Hansen JA. A 44 kilodalton cell surface homodimer regulates interleukin 2 production by activated human T lymphocytes. J Immunol. 1986;136(9):3282–87. PMID: 3082984. doi:10.4049/jimmunol.136.9.3282.
  • Weiss A, Manger B, Imboden J. Synergy between the T3/antigen receptor complex and Tp44 in the activation of human T cells. J Immunol. 1986;137(3):819–25. PMID: 3088111.
  • Damle NK, Mohagheghpour N, Hansen JA, Engleman EG. Alloantigen-specific cytotoxic and suppressor T lymphocytes are derived from phenotypically distinct precursors. J Immunol. 1983;131:2296–300. doi:10.4049/jimmunol.131.5.2296. PMID: 6195259.
  • Siokis A, Robert PA, Demetriou P, Dustin ML, Meyer-Hermann M. F-Actin-Driven CD28-CD80 localization in the immune synapse. Cell Rep. 2018;24:1151–62. doi:10.1016/j.celrep.2018.06.114. PMID: 30067972.
  • Freeman GJ, Freedman AS, Segil JM, Lee G, Whitman JF, Nadler LM. B7, a new member of the Ig superfamily with unique expression on activated and neoplastic B cells. J Immunol. 1989;143(8):2714–22. PMID: 2794510. doi:10.4049/jimmunol.143.8.2714.
  • Freeman GJ, Borriello F, Hodes RJ, Reiser H, Gribben JG, Ng JW, Kim J, Goldberg JM, Hathcock K, Laszlo G, et al. Murine B7-2, an alternative CTLA4 counter-receptor that costimulates T cell proliferation and interleukin 2 production. J Exp Med. 1993;178(6):2185–92. doi:10.1084/jem.178.6.2185. PMID: 7504059.
  • Freeman GJ, Gribben JG, Boussiotis VA, Ng JW, Restivo VA Jr., Lombard LA, Gray GS, Nadler LM. Cloning of B7-2: a CTLA-4 counter-receptor that costimulates human T cell proliferation. Science. 1993;262:909–11. PMID: 7694363. doi:10.1126/science.7694363.
  • Caux C, Vanbervliet B, Massacrier C, Azuma M, Okumura K, Lanier LL, Banchereau J. B70/B7-2 is identical to CD86 and is the major functional ligand for CD28 expressed on human dendritic cells. J Exp Med. 1994;180:1841–47. doi:10.1084/jem.180.5.1841. PMID: 7525840.
  • Singh A, Dees S, Grewal IS. Overcoming the challenges associated with CD3+ T-cell redirection in cancer. Br J Cancer. 2021;124:1037–48. doi:10.1038/s41416-020-01225-5. PMID: 33469153.
  • Eshhar Z, Waks T, Gross G, Schindler DG. Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc Natl Acad Sci U S A. 1993;90(2):720–24. PMID: 8421711. doi:10.1073/pnas.90.2.720.
  • Brocker T, Karjalainen K. Signals through T cell receptor-zeta chain alone are insufficient to prime resting T lymphocytes. J Exp Med. 1995;181(5):1653–59. PMID: 7722445. doi:10.1084/jem.181.5.1653.
  • Till BG, Jensen MC, Wang J, Chen EY, Wood BL, Greisman HA, Qian X, James SE, Raubitschek A, Forman SJ, et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood. 2008;112:2261–71. doi:10.1182/blood-2007-12-128843. PMID: 18509084.
  • Krause A, Guo HF, Latouche JB, Tan C, Cheung NK, Sadelain M. Antigen-dependent CD28 signaling selectively enhances survival and proliferation in genetically modified activated human primary T lymphocytes. J Exp Med. 1998;188:619–26. doi:10.1084/jem.188.4.619. PMID: 9705944.
  • Sadelain M, Brentjens R, Rivière I. The basic principles of chimeric antigen receptor design. Cancer Discov. 2013;3:388–98. doi:10.1158/2159-8290.Cd-12-0548. PMID: 23550147.
  • Locke FL, Neelapu SS, Bartlett NL, Siddiqi T, Chavez JC, Hosing CM, Ghobadi A, Budde LE, Bot A, Rossi JM, et al. Phase 1 Results of ZUMA-1: a Multicenter Study of KTE-C19 Anti-CD19 CAR T Cell Therapy in Refractory Aggressive Lymphoma. Mol Ther. 2017;25:285–95. doi:10.1016/j.ymthe.2016.10.020. PMID: 28129122.
  • Neelapu SS, Locke FL, Bartlett NL, Lekakis LJ, Miklos DB, Jacobson CA, Braunschweig I, Oluwole OO, Siddiqi T, Lin Y, et al. Axicabtagene ciloleucel CAR T-Cell therapy in refractory large B-Cell lymphoma. N Engl J Med. 2017;377:2531–44. doi:10.1056/NEJMoa1707447. PMID: 29226797.
  • Laszlo GS, Gudgeon CJ, Harrington KH, Walter RB. T-cell ligands modulate the cytolytic activity of the CD33/CD3 BiTE antibody construct, AMG 330. Blood Cancer J. 2015;5:e340. PMID: 26295610. doi:10.1038/bcj.2015.68.
  • Skokos D, Waite JC, Haber L, Crawford A, Hermann A, Ullman E, Slim R, Godin S, Ajithdoss D, Ye X, et al. A class of costimulatory CD28-bispecific antibodies that enhance the antitumor activity of CD3-bispecific antibodies. Sci Transl Med. PMID: 31915305, 2020;12. doi:10.1126/scitranslmed.aaw7888.
  • Wei J, Yang Y, Wang G, Liu M. Current landscape and future directions of bispecific antibodies in cancer immunotherapy. Front Immunol. 2022;13:1035276. doi:10.3389/fimmu.2022.1035276. PMID: 36389699.
  • Suntharalingam G, Perry MR, Ward S, Brett SJ, Castello-Cortes A, Brunner MD, Panoskaltsis N. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N Engl J Med. 2006;355:1018–28. doi:10.1056/NEJMoa063842. PMID: 16908486.
  • Tacke M, Hanke G, Hanke T, Hünig T. CD28-mediated induction of proliferation in resting T cells in vitro and in vivo without engagement of the T cell receptor: evidence for functionally distinct forms of CD28. Eur J Immunol. 1997;27(1):239–47. PMID: 9022025. doi:10.1002/eji.1830270136.
  • Lühder F, Huang Y, Dennehy KM, Guntermann C, Müller I, Winkler E, Kerkau T, Ikemizu S, Davis SJ, Hanke T, et al. Topological requirements and signaling properties of T cell–activating, anti-CD28 antibody superagonists. J Exp Med. 2003;197(8):955–66. doi:10.1084/jem.20021024. PMID: 12707299.
  • Rodríguez-Palmero M, Hara T, Thumbs A, Hünig T. Triggering of T cell proliferation through CD28 induces GATA-3 and promotes T helper type 2 differentiation in vitro and in vivo. Eur J Immunol. 1999;29:3914–24. PMID: 10601999. doi:10.1002/(sici)1521-4141(199912)29:12<3914:Aid:12<3914:Aidimmu3914>3.0.Co;20.Co;2#.
  • Pallardy M, Hünig T. Primate testing of TGN1412: right target, wrong cell. Br J Pharmacol. 2010;161:509–11. doi:10.1111/j.1476-5381.2010.00925.x. PMID: 20880391.
  • Hanke T. Lessons from TGN1412. Lancet. 2006;368(9547):1569–70. author reply 1570 PMID: 17084746. doi:10.1016/s0140-6736(06)69651-7.
  • Römer PS, Berr S, Avota E, Na SY, Battaglia M, ten Berge I, Einsele H, Hünig T. Preculture of PBMCs at high cell density increases sensitivity of T-cell responses, revealing cytokine release by CD28 superagonist TGN1412. Blood. 2011;118:6772–82. doi:10.1182/blood-2010-12-319780. PMID: 21931118.
  • Eastwood D, Findlay L, Poole S, Bird C, Wadhwa M, Moore M, Burns C, Thorpe R, Stebbings R. Monoclonal antibody TGN1412 trial failure explained by species differences in CD28 expression on CD4+ effector memory T-cells. Br J Pharmacol. 2010;161:512–26. doi:10.1111/j.1476-5381.2010.00922.x. PMID: 20880392.
  • Horvath CJ, Milton MN. The TeGenero incident and the Duff Report conclusions: a series of unfortunate events or an avoidable event? Toxicol Pathol. 2009;37:372–83. doi:10.1177/0192623309332986. PMID: 19244218.
  • Hünig T. The storm has cleared: lessons from the CD28 superagonist TGN1412 trial. Nat Rev Immunol. 2012;12:317–18. doi:10.1038/nri3192. PMID: 22487653.
  • Horvath C, Andrews L, Baumann A, Black L, Blanset D, Cavagnaro J, Hastings KL, Hutto DL, MacLachlan TK, Milton M, et al. Storm forecasting: additional lessons from the CD28 superagonist TGN1412 trial. Nat Rev Immunol. 2012;12:740. doi:10.1038/nri3192-c1. author reply 740 PMID: 22941443.
  • Ye C, Yang H, Cheng M, Shultz LD, Greiner DL, Brehm MA, Keck JG. A rapid, sensitive, and reproducible in vivo PBMC humanized murine model for determining therapeutic-related cytokine release syndrome. FASEB J. 2020;34:12963–75. PMID: 32772418. doi:10.1096/fj.202001203R.
  • Peissert F, Plüss L, Giudice AM, Ongaro T, Villa A, Elsayed A, Nadal L, Dakhel Plaza S, Scietti L, Puca E, et al. Selection of a PD-1 blocking antibody from a novel fully human phage display library. Protein Sci. 2022;31:e4486. PMID: 36317676. doi:10.1002/pro.4486.
  • Nagano K, Tsutsumi Y. Phage display technology as a powerful platform for antibody drug discovery. Viruses. 2021;13(2). PMID: 33504115. doi:10.3390/v13020178.
  • Evans EJ, Esnouf RM, Manso-Sancho R, Gilbert RJ, James JR, Yu C, Fennelly JA, Vowles C, Hanke T, Walse B, et al. Crystal structure of a soluble CD28-Fab complex. Nat Immunol. 2005;6:271–79. doi:10.1038/ni1170. PMID: 15696168.
  • Frank R. The SPOT-synthesis technique. Synthetic peptide arrays on membrane supports--principles and applications. J Immunol Methods. 2002;267(1):13–26. PMID: 12135797. doi:10.1016/s0022-1759(02)00137-0.
  • Malek TR. The biology of interleukin-2. Annu Rev Immunol. 2008;26:453–79. doi:10.1146/annurev.immunol.26.021607.090357. PMID: 18062768.
  • Boyman O, Sprent J. The role of interleukin-2 during homeostasis and activation of the immune system. Nat Rev Immunol. 2012;12:180–90. doi:10.1038/nri3156. PMID: 22343569.
  • Kaspar M, Zardi L, Neri D. Fibronectin as target for tumor therapy. Int J Cancer. 2006;118:1331–39. doi:10.1002/ijc.21677. PMID: 16381025.
  • Esensten JH, Helou YA, Chopra G, Weiss A, Bluestone JA. CD28 costimulation: from mechanism to therapy. Immunity. 2016;44:973–88. doi:10.1016/j.immuni.2016.04.020. PMID: 27192564.
  • Stebbings R, Findlay L, Edwards C, Eastwood D, Bird C, North D, Mistry Y, Dilger P, Liefooghe E, Cludts I, et al. “Cytokine storm” in the phase I trial of monoclonal antibody TGN1412: better understanding the causes to improve preclinical testing of immunotherapeutics. J Immunol. 2007;179:3325–31. doi:10.4049/jimmunol.179.5.3325. PMID: 17709549.
  • Morillon YM 2nd, Sabzevari A, Schlom J, Greiner JW. The development of next-generation PBMC humanized mice for preclinical investigation of cancer immunotherapeutic agents. Anticancer Res. 2020;40:5329–41. PMID: 32988851. doi:10.21873/anticanres.14540.
  • Spitaleri G, Berardi R, Pierantoni C, De Pas T, Noberasco C, Libbra C, González-Iglesias R, Giovannoni L, Tasciotti A, Neri D, et al. Phase I/II study of the tumour-targeting human monoclonal antibody–cytokine fusion protein L19-TNF in patients with advanced solid tumours. J Cancer Res Clin Oncol. 2013;139(3):447–55. doi:10.1007/s00432-012-1327-7. PMID: 23160853.
  • Schwager K, Hemmerle T, Aebischer D, Neri D. The immunocytokine L19–IL2 eradicates cancer when used in combination with CTLA-4 blockade or with L19-TNF. J Invest Dermatol. 2013;133(3):751–58. PMID: 23096716. doi:10.1038/jid.2012.376.
  • Danielli R, Patuzzo R, Di Giacomo AM, Gallino G, Maurichi A, Di Florio A, Cutaia O, Lazzeri A, Fazio C, Miracco C, et al. Intralesional administration of L19-IL2/L19-TNF in stage III or stage IVM1a melanoma patients: results of a phase II study. Cancer Immunol Immunother. 2015;64:999–1009. doi:10.1007/s00262-015-1704-6. PMID: 25971540.
  • Millul J, Bassi G, Mock J, Elsayed A, Pellegrino C, Zana A, Dakhel Plaza S, Nadal L, Gloger A, Schmidt E, et al.An ultra-high-affinity small organic ligand of fibroblast activation protein for tumor-targeting applicationsProc Natl Acad Sci U S A202111810.1073/pnas.2101852118 PMID: 3385002416
  • Rajendra Y, Kiseljak D, Baldi L, Hacker DL, Wurm FM. A simple high-yielding process for transient gene expression in CHO cells. J Biotechnol. 2011;153:22–26. doi:10.1016/j.jbiotec.2011.03.001. PMID: 21392548.
  • Fairhead M, Howarth M. Site-specific biotinylation of purified proteins using BirA. Methods Mol Biol. 2015;1266:171–84. PMID: 25560075. doi:10.1007/978-1-4939-2272-7_12.
  • Viti F, Nilsson F, Demartis S, Huber A, Neri D. Design and use of phage display libraries for the selection of antibodies and enzymes. Methods Enzymol. 2000;326:480–505. PMID: 11036659. doi:10.1016/s0076-6879(00)26071-0.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.