Failure to upregulate cell surface PD-1 is associated with dysregulated stimulation of T cells by TGN1412-like CD28 superagonist

References

• Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12:252-64; PMID:22437870; http://dx.doi.org/10.1038/nrc3239
   PubMed Web of Science ®Google Scholar
• Gray JC, Johnson PW, Glennie MJ. Therapeutic potential of immunostimulatory monoclonal antibodies. Clin Sci (Lond) 2006; 111:93-106; PMID:16831129; http://dx.doi.org/10.1042/CS20060024
   PubMed Web of Science ®Google Scholar
• 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; PMID:16908486; http://dx.doi.org/10.1056/NEJMoa063842
   PubMed Web of Science ®Google Scholar
• 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; PMID:17709549; http://dx.doi.org/10.4049/jimmunol.179.5.3325
   PubMed Web of Science ®Google Scholar
• Waibler Z, Sender LY, Merten C, Hartig R, Kliche S, Gunzer M, Reichardt P, Kalinke U, Schraven B. Signaling signatures and functional properties of anti-human CD28 superagonistic antibodies. PLoS One 2008; 3:e1708; PMID:18320029; http://dx.doi.org/10.1371/journal.pone.0001708
   PubMed Web of Science ®Google Scholar
• Thaventhiran T, Sethu S, Yeang HXA, Al-Huseini L, Hamdam J, Sathish JG. T Cell Co-inhibitory Receptors: Functions and Signalling Mechanisms. Journal of Clinical and Cellular Immunology 2012; S12
   Google Scholar
• Jin HT, Ahmed R, Okazaki T. Role of PD-1 in regulating T-cell immunity. Curr Top Microbiol Immunol 2011; 350:17-37; PMID:21061197; http://dx.doi.org/10.1007/82_2010_116
   PubMed Web of Science ®Google Scholar
• Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008; 26:677-704; PMID:18173375; http://dx.doi.org/10.1146/annurev.immunol.26.021607.090331
   PubMed Web of Science ®Google Scholar
• Wei F, Zhong S, Ma Z, Kong H, Medvec A, Ahmed R, Freeman GJ, Krogsgaard M, Riley JL. Strength of PD-1 signaling differentially affects T-cell effector functions. Proc Natl Acad Sci U S A 2013; 110:E2480-9; PMID:23610399; http://dx.doi.org/10.1073/pnas.1305394110
   PubMed Web of Science ®Google Scholar
• 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; PMID:20880392; http://dx.doi.org/10.1111/j.1476-5381.2010.00922.x
   PubMed Web of Science ®Google Scholar
• 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; PMID:21931118; http://dx.doi.org/10.1182/blood-2010-12-319780
   PubMed Web of Science ®Google Scholar
• San José E, Borroto A, Niedergang F, Alcover A, Alarcón B. Triggering the TCR complex causes the downregulation of nonengaged receptors by a signal transduction-dependent mechanism. Immunity 2000; 12:161-70; PMID:10714682; http://dx.doi.org/10.1016/S1074-7613(00)80169-7
   PubMed Web of Science ®Google Scholar
• Hedfors IA, Brinchmann JE. Long-term proliferation and survival of in vitro-activated T cells is dependent on Interleukin-2 receptor signalling but not on the high-affinity IL-2R. Scand J Immunol 2003; 58:522-32; PMID:14629624; http://dx.doi.org/10.1046/j.1365-3083.2003.01338.x
   PubMed Web of Science ®Google Scholar
• Eastwood D, Bird C, Dilger P, Hockley J, Findlay L, Poole S, Thorpe SJ, Wadhwa M, Thorpe R, Stebbings R. Severity of the TGN1412 trial disaster cytokine storm correlated with IL-2 release. Br J Clin Pharmacol 2013; 76:299-315; PMID:23701319; http://dx.doi.org/10.1111/bcp.12165
   PubMed Web of Science ®Google Scholar
• Marelli-Berg FM, Okkenhaug K, Mirenda V. A two-signal model for T cell trafficking. Trends Immunol 2007; 28:267-73; PMID:17481953; http://dx.doi.org/10.1016/j.it.2007.04.008
   PubMed Web of Science ®Google Scholar
• Smith A, Bracke M, Leitinger B, Porter JC, Hogg N. LFA-1-induced T cell migration on ICAM-1 involves regulation of MLCK-mediated attachment and ROCK-dependent detachment. J Cell Sci 2003; 116:3123-33; PMID:12799414; http://dx.doi.org/10.1242/jcs.00606
   PubMed Web of Science ®Google Scholar
• Oak JS, Fruman DA. Role of phosphoinositide 3-kinase signaling in autoimmunity. Autoimmunity 2007; 40:433-41; PMID:17729037; http://dx.doi.org/10.1080/08916930701464780
   PubMed Web of Science ®Google Scholar
• Leslie NR. PTEN: an intercellular peacekeeper? Sci Signal 2012; 5:pe50; PMID:23150879; http://dx.doi.org/10.1126/scisignal.2003685
   PubMed Web of Science ®Google Scholar
• Patsoukis N, Li L, Sari D, Petkova V, Boussiotis VA. PD-1 increases PTEN phosphatase activity while decreasing PTEN protein stability by inhibiting casein kinase 2. Mol Cell Biol 2013; 33:3091-8; PMID:23732914; http://dx.doi.org/10.1128/MCB.00319-13
   PubMed Web of Science ®Google Scholar
• Gourley TS, Chang CH. Cutting edge: the class II transactivator prevents activation-induced cell death by inhibiting Fas ligand gene expression. J Immunol 2001; 166:2917-21; PMID:11207239; http://dx.doi.org/10.4049/jimmunol.166.5.2917
   PubMed Web of Science ®Google Scholar
• Zhang X, Nakajima T, Goronzy JJ, Weyand CM. Tissue trafficking patterns of effector memory CD4+ T cells in rheumatoid arthritis. Arthritis Rheum 2005; 52:3839-49; PMID:16329093; http://dx.doi.org/10.1002/art.21482
   PubMed Web of Science ®Google Scholar
• Sandilands GP, Wilson M, Huser C, Jolly L, Sands WA, McSharry C. Were monocytes responsible for initiating the cytokine storm in the TGN1412 clinical trial tragedy? Clin Exp Immunol 2010; 162:516-27; PMID:20964641; http://dx.doi.org/10.1111/j.1365-2249.2010.04264.x
   PubMed Web of Science ®Google Scholar
• Hogg N, Patzak I, Willenbrock F. The insider's guide to leukocyte integrin signalling and function. Nat Rev Immunol 2011; 11:416-26; PMID:21597477; http://dx.doi.org/10.1038/nri2986
   PubMed Web of Science ®Google Scholar
• Iliopoulos D, Kavousanaki M, Ioannou M, Boumpas D, Verginis P. The negative costimulatory molecule PD-1 modulates the balance between immunity and tolerance via miR-21. Eur J Immunol 2011; 41:1754-63; PMID:21469086; http://dx.doi.org/10.1002/eji.201040646
   PubMed Web of Science ®Google Scholar
• Pentcheva-Hoang T, Chen L, Pardoll DM, Allison JP. Programmed death-1 concentration at the immunological synapse is determined by ligand affinity and availability. Proc Natl Acad Sci U S A 2007; 104:17765-70; PMID:17968013; http://dx.doi.org/10.1073/pnas.0708767104
   PubMed Web of Science ®Google Scholar
• Medina-Tato DA, Ward SG, Watson ML. Phosphoinositide 3-kinase signalling in lung disease: leucocytes and beyond. Immunology 2007; 121:448-61; PMID:17614878; http://dx.doi.org/10.1111/j.1365-2567.2007.02663.x
   PubMed Web of Science ®Google Scholar
• Sathish JG, Sethu S, Bielsky MC, de Haan L, French NS, Govindappa K, Green J, Griffiths CE, Holgate S, Jones D, et al. Challenges and approaches for the development of safer immunomodulatory biologics. Nat Rev Drug Discov 2013; 12:306-24; PMID:23535934; http://dx.doi.org/10.1038/nrd3974
   PubMed Web of Science ®Google Scholar
• Ball C, Fox B, Hufton S, Sharp G, Poole S, Stebbings R, Eastwood D, Findlay L, Parren PW, Thorpe R, et al. Antibody C region influences TGN1412-like functional activity in vitro. J Immunol 2012; 189:5831-40; PMID:23150712; http://dx.doi.org/10.4049/jimmunol.1201795
   PubMed Web of Science ®Google Scholar