Antibody-peptide-MHC fusion conjugates target non-cognate T cells to kill tumour cells

Cancer Immunology, Immunotherapy

Volumn 62, Issue 6, 2013, Pages 1093-1105

  King, Ben C ^a   Hamblin, Angela D ^a   Savage, Philip M ^c   Douglas, Leon R ^b   Hansen, Ted H ^d   French, Ruth R ^a   Johnson, Peter W M ^b   Glennie, Martin J ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b SOUTHAMPTON GENERAL HOSPITAL   (United Kingdom)

^c CHARING CROSS HOSPITAL   (United Kingdom)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antibody peptide MHC conjugates; Immunotherapy; Retargeting non cognate cytotoxic T cells; Single chain trimer

Indexed keywords

BETA 2 MICROGLOBULIN; BISPECIFIC ANTIBODY; CD20 ANTIGEN; CD3 ANTIGEN; CD8 ANTIGEN; IMMUNOGLOBULIN F(AB) FRAGMENT; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL KILLING; CONJUGATION; CONTROLLED STUDY; CROSS LINKING; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TUMOR CELL;

ANIMALS; ANTIBODIES, BISPECIFIC; ANTIGENS, CD20; B-LYMPHOCYTES; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; GENE ORDER; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOCONJUGATES; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MICE; NEOPLASMS; OVALBUMIN; PEPTIDES; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; SINGLE-CHAIN ANTIBODIES; T-LYMPHOCYTES; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84878847720     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-013-1408-8     Document Type: Article

References (41)

1. Warren EH, Fujii N, Akatsuka Y, Chaney CN, Mito JK, Loeb KR, Gooley TA, Brown ML, Koo KK, Rosinski KV, Ogawa S, Matsubara A, Appelbaum FR, Riddell SR (2010) Therapy of relapsed leukemia after allogeneic hematopoietic cell transplantation with T cells specific for minor histocompatibility antigens. Blood 115:3869-3878. doi: 10.1182/blood-2009-10-248997
2. Sheikh NA, Petrylak D, Kantoff PW, Dela Rosa C, Stewart FP, Kuan LY, Whitmore JB, Trager JB, Poehlein CH, Frohlich MW, Urdal DL (2012) Sipuleucel-T immune parameters correlate with survival: an analysis of the randomized phase 3 clinical trials in men with castration-resistant prostate cancer. Cancer Immunol Immunother 62:137-147. doi: 10.1007/s00262-012-1317-2
3. Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, Kammula U, Robbins PF, Huang J, Citrin DE, Leitman SF, Wunderlich J, Restifo NP, Thomasian A, Downey SG, Smith FO, Klapper J, Morton K, Laurencot C, White DE, Rosenberg SA (2008) Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 26:5233-5239. doi: 10.1200/JCO.2008.16.5449
4. Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME (2008) Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 8:299-308. doi: 10.1038/ncr2355
5. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, Citrin DE, Restifo NP, Robbins PF, Wunderlich JR, Morton KE, Laurencot CM, Steinberg SM, White DE, Dudley ME (2011) Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 17:4550-4557. doi: 10.1158/1078-0432.CCR-11-0116
6. Jorritsma A, Schotte R, Coccoris M, de Witte MA, Schumacher TN (2011) Prospects and limitations of T cell receptor gene therapy. Curr Gene Ther 11:276-287. doi: 10.2174/156652311796150390
7. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, Royal RE, Topalian SL, Kammula US, Restifo NP, Zheng Z, Nahvi A, de Vries CR, Rogers-Freezer LJ, Mavroukakis SA, Rosenberg SA (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314:126-129. doi: 10.1126/science.1129003
8. Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, Hughes MS, Kammula US, Royal RE, Sherry RM, Wunderlich JR, Lee CC, Restifo NP, Schwarz SL, Cogdill AP, Bishop RJ, Kim H, Brewer CC, Rudy SF, VanWaes C, Davis JL, Mathur A, Ripley RT, Nathan DA, Laurencot CM, Rosenberg SA (2009) Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114:535-546. doi: 10.1182/blood-2009-03-211714
9. Parkhurst MR, Yang JC, Langan RC, Dudley ME, Nathan DA, Feldman SA, Davis JL, Morgan RA, Merino MJ, Sherry RM, Hughes MS, Kammula US, Phan GQ, Lim RM, Wank SA, Restifo NP, Robbins PF Laurencot CM, Rosenberg SA (2011) T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther 19:620-626. doi: 10.1038/mt.2010.272
10. Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, Wunderlich JR, Nahvi AV, Helman LJ, Mackall CL, Kammula US, Hughes MS, Restifo NP, Raffeld M, Lee CC, Levy CL, Li YF, El-Gamil M, Schwarz SL, Laurencot C, Rosenberg SA (2011) Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 29:917-924. doi: 10.1200/JCO.2010.32.2537
11. Morgan RA, Dudley ME, Rosenberg SA (2010) Adoptive cell therapy: genetic modification to redirect effector cell specificity. Cancer J 16:336-341. doi: 10.1097/PPO.0b013e3181eb3879
12. Kalos M, Levine BL, Porter DL, Katz S, Grupp SA, Bagg A, June CH (2011) T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Science translational medicine 3:95ra73. doi: 10.1126/scitranslmed.3002842
13. Tibben JG, Boerman OC, Massuger LF, Schijf CP, Claessens RA, Corstens FH (1996) Pharmacokinetics, biodistribution and biological effects of intravenously administered bispecific monoclonal antibody OC/TR F(ab′)2 in ovarian carcinoma patients. Int J Cancer 66:477-483. doi: 10.1002/(SICI)1097- 0215(19960516)66:4<477:AID-IJC11>3.0.CO;2-5
14. Bargou R, Leo E, Zugmaier G, Klinger M, Goebeler M, Knop S, Noppeney R, Viardot A, Hess G, Schuler M, Einsele H, Brandl C, Wolf A, Kirchinger P, Klappers P, Schmidt M, Riethmuller G, Reinhardt C, Baeuerle PA, Kufer P (2008) Tumor regression in cancer patients by very low doses of a T cell-engaging antibody. Science 321:974-977. doi: 10.1126/science.1158545
15. Topp MS, Kufer P, Gokbuget N, Goebeler M, Klinger M, Neumann S, Horst HA, Raff T, Viardot A, Schmid M, Stelljes M, Schaich M, Degenhard E, Kohne-Volland R, Bruggemann M, Ottmann O, Pfeifer H, Burmeister T, Nagorsen D, Schmidt M, Lutterbuese R, Reinhardt C, Baeuerle PA, Kneba M, Einsele H, Riethmuller G, Hoelzer D, Zugmaier G, Bargou RC (2011) Targeted therapy with the T-cell-engaging antibody blinatumomab of chemotherapy-refractory minimal residual disease in B-lineage acute lymphoblastic leukemia patients results in high response rate and prolonged leukemia-free survival. J Clin Oncol 29:2493-2498. doi: 10.1200/JCO.2010.32.7270
16. Went P, Vasei M, Bubendorf L, Terracciano L, Tornillo L, Riede U, Kononen J, Simon R, Sauter G, Baeuerle PA (2006) Frequent high-level expression of the immunotherapeutic target Ep-CAM in colon, stomach, prostate and lung cancers. Br J Cancer 94:128-135. doi: 10.1038/sj.bjc.6602924
17. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, Hoey T, Gurney A, Huang EH, Simeone DM, Shelton AA, Parmiani G, Castelli C, Clarke MF (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 104:10158-10163. doi: 10.1073/pnas.0703478104
18. Cioffi M, Dorado J, Baeuerle PA, Heeschen C (2012) EpCAM/CD3-Bispecific T-cell engaging antibody MT110 eliminates primary human pancreatic cancer stem cells. Clin Cancer Res 18:465-474. doi: 10.1158/1078-0432.CCR-11-1270
19. Yu YY, Netuschil N, Lybarger L, Connolly JM, Hansen TH (2002) Cutting edge: single-chain trimers of MHC class I molecules form stable structures that potently stimulate antigen-specific T cells and B cells. J Immunol 168:3145-3149
20. Hansen TH, Connolly JM, Gould KG, Fremont DH (2010) Basic and translational applications of engineered MHC class I proteins. Trends Immunol 31:363-369. doi: 10.1016/j.it.2010.07.003
21. Beers SA, Chan CH, James S, French RR, Attfield KE, Brennan CM, Ahuja A, Shlomchik MJ, Cragg MS, Glennie MJ (2008) Type II (tositumomab) anti-CD20 monoclonal antibody out performs type I (rituximab-like) reagents in B-cell depletion regardless of complement activation. Blood 112:4170-4177. doi: 10.1182/blood-2008-04-149161
22. Chan HT, Hughes D, French RR, Tutt AL, Walshe CA, Teeling JL, Glennie MJ, Cragg MS (2003) CD20-induced lymphoma cell death is independent of both caspases and its redistribution into triton X-100 insoluble membrane rafts. Cancer Res 63:5480-5489
23. Porgador A, Yewdell JW, Deng Y, Bennink JR, Germain RN (1997) Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 6:715-726. doi: 10.1016/S1074-7613(00)80447-1
24. Tutt AL, French RR, Illidge TM, Honeychurch J, McBride HM, Penfold CA, Fearon DT, Parkhouse RM, Klaus GG, Glennie MJ (1998) Monoclonal antibody therapy of B cell lymphoma: signaling activity on tumor cells appears more important than recruitment of effectors. J Immunol 161:3176-3185
25. Lybarger L, Yu YY, Miley MJ, Fremont DH, Myers N, Primeau T, Truscott SM, Connolly JM, Hansen TH (2003) Enhanced immune presentation of a single-chain major histocompatibility complex class I molecule engineered to optimize linkage of a C-terminally extended peptide. J Biol Chem 278:27105-27111. doi: 10.1074/jbc.M303716200
26. Glennie MJ, McBride HM, Worth AT, Stevenson GT (1987) Preparation and performance of bispecific F(ab′ gamma)2 antibody containing thioether-linked Fab′ gamma fragments. J Immunol 139:2367-2375
27. French RR (2000) How to make bispecific antibodies. Methods Mol Med 40:333-339. doi: 10.1007/978-1-59259-076-6-26
28. Donda A, Cesson V, Mach JP, Corradin G, Primus FJ, Robert B (2003) In vivo targeting of an anti-tumor antibody coupled to antigenic MHC class I complexes induces specific growth inhibition and regression of established syngeneic tumor grafts. Cancer Immun 3:11
29. Ogg GS, Dunbar PR, Cerundolo V, McMichael AJ, Lemoine NR, Savage P (2000) Sensitization of tumour cells to lysis by virus-specific CTL using antibody-targeted MHC class I/peptide complexes. Br J Cancer 82:1058-1062. doi: 10.1054/bjoc.1999.1042
30. Mous R, Savage P, Remmerswaal EB, van Lier RA, Eldering E, van Oers MH (2006) Redirection of CMV-specific CTL towards B-CLL via CD20-targeted HLA/CMV complexes. Leukemia 20:1096-1102. doi: 10.1038/sj.leu.2404185
31. Savage P, Dyson J, Milrain M, Mathews D, King B, Chan HT, Barber L, Epenetos A, Ogg G, McMichael A, Glennie MJ, French RR (2007) Immunotherapy with antibody-targeted HLA class I complexes: results of in vivo cell killing and therapeutic vaccination. Tumour Biol 28:205-211. doi: 10.1159/000107416
32. Savage P, Cowburn P, Clayton A, Man S, Lawson T, Ogg G, Lemoine N, McMichael A, Epenetos A (2002) Anti-viral cytotoxic T cells inhibit the growth of cancer cells with antibody targeted HLA class I/peptide complexes in SCID mice. Int J Cancer 98:561-566. doi: 10.1002/ijc.10219
33. Robert B, Guillaume P, Luescher I, Romero P, Mach JP (2000) Antibody-conjugated MHC class I tetramers can target tumor cells for specific lysis by T lymphocytes. Eur J Immunol 30:3165-3170. doi: 10.1002/1521- 4141(200011)30:11<3165:AID-IMMU3165>3.0.CO;2-R
34. Knox SJ, Goris ML, Tempero M, Weiden PL, Gentner L, Breitz H, Adams GP, Axworthy D, Gaffigan S, Bryan K, Fisher DR, Colcher D, Horak ID, Weiner LM (2000) Phase II trial of yttrium-90-DOTA-biotin pretargeted by NR-LU-10 antibody/streptavidin in patients with metastatic colon cancer. Clin Cancer Res 6:406-414
35. Forero A, Weiden PL, Vose JM, Knox SJ, LoBuglio AF, Hankins J, Goris ML, Picozzi VJ, Axworthy DB, Breitz HB, Sims RB, Ghalie RG, Shen S, Meredith RF (2004) Phase 1 trial of a novel anti-CD20 fusion protein in pretargeted radioimmunotherapy for B-cell non-Hodgkin lymphoma. Blood 104:227-236. doi: 10.1182/blood-2003-09-3284
36. Robert B, Guillaume P, Luescher I, Doucey MA, Cerottini JC, Romero P, Mach JP (2001) Redirecting anti-viral CTL against cancer cells by surface targeting of monomeric MHC class I-viral peptide conjugated to antibody fragments. Cancer Immun 1:2
37. Cesson V, Stirnemann K, Robert B, Luescher I, Filleron T, Corradin G, Mach JP, Donda A (2006) Active antiviral T-lymphocyte response can be redirected against tumor cells by antitumor antibody × MHC/viral peptide conjugates. Clin Cancer Res 12:7422-7430. doi: 10.1158/1078-0432.CCR-06-1862
38. Ge Q, Stone JD, Thompson MT, Cochran JR, Rushe M, Eisen HN, Chen J, Stern LJ (2002) Soluble peptide-MHC monomers cause activation of CD8+ T cells through transfer of the peptide to T cell MHC molecules. Proc Natl Acad Sci USA 99:13729-13734. doi: 10.1073/pnas.212515299
39. Lev A, Noy R, Oved K, Novak H, Segal D, Walden P, Zehn D, Reiter Y (2004) Tumor-specific Ab-mediated targeting of MHC-peptide complexes induces regression of human tumor xenografts in vivo. Proc Natl Acad Sci USA 101:9051-9056. doi: 10.1073/pnas.0403222101
40. Ma Z, Sharp KA, Janmey PA, Finkel TH (2008) Surface-anchored monomeric agonist pMHCs alone trigger TCR with high sensitivity. PLoS Biol 6:e43. doi: 10.1371/journal.pbio.0060043
41. Stevenson FK, Ottensmeier CH, Johnson P, Zhu D, Buchan SL, McCann KJ, Roddick JS, King AT, McNicholl F, Savelyeva N, Rice J (2004) DNA vaccines to attack cancer. Proc Natl Acad Sci USA 101(Suppl 2):14646-14652. doi: 10.1073/pnas.0404896101