T-cell responses against CD19+ pediatric acute lymphoblastic leukemia mediated by bispecific T-cell engager (BiTE) are regulated contrarily by PD-L1 and CD80/CD86 on leukemic blasts

Oncotarget

Volumn 7, Issue 47, 2016, Pages 76902-76919

  Feucht, Judith ^a,b   Kayser, Simone ^a   Gorodezki, David ^a   Hamieh, Mohamad ^b   Döring, Michaela ^a,c   Blaeschke, Franziska ^c   Schlegel, Patrick ^a   Bösmüller, Hans ^a   Quintanilla Fend, Leticia ^a   Ebinger, Martin ^a   Lang, Peter ^a   Handgretinger, Rupert ^a   Feuchtinger, Tobias ^a,c  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

Blinatumomab; CD80 86; Immune checkpoints; PD L1; Pediatric acute lymphoblastic leukemia; T cells

Indexed keywords

B7 ANTIGEN; BLINATUMOMAB; C REACTIVE PROTEIN; CD19 ANTIGEN; CD27 ANTIGEN; CD3 ANTIGEN; CD40 ANTIGEN; CD70 ANTIGEN; CD86 ANTIGEN; D DIMER; FERRITIN; HERPESVIRUS ENTRY MEDIATOR; INTERLEUKIN 6; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PEMBROLIZUMAB; PROCALCITONIN; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; SOLUBLE INTERLEUKIN 2 RECEPTOR; BISPECIFIC ANTIBODY; MONOCLONAL ANTIBODY; TUMOR MARKER;

ABNORMALLY HIGH SUBSTRATE CONCENTRATION IN BLOOD; ACUTE LYMPHOBLASTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER REGRESSION; CELL EXPANSION; CHILD; CLINICAL ARTICLE; COCULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG RESPONSE; DRUG SAFETY; EFFECTOR CELL; FEASIBILITY STUDY; FEMALE; FEVER; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; PROTEIN EXPRESSION; RAJI CELL LINE; SCHOOL CHILD; T LYMPHOCYTE; TARGET CELL; UPREGULATION; CELL PROLIFERATION; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; TUMOR CELL LINE;

ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD19; BIOMARKERS, TUMOR; CELL LINE, TUMOR; CELL PROLIFERATION; CHILD; FEMALE; HUMANS; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; T-LYMPHOCYTES;

EID: 84998886281     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12357     Document Type: Article

References (46)

1. Hunger SP, Lu X, Devidas M, Camitta BM, Gaynon PS, Winick NJ, Reaman GH and Carroll WL. Improved survival for children and adolescents with acute lymphoblastic leukemia between 1990 and 2005: a report from the children's oncology group. J Clin Oncol. 2012; 30:1663-1669.
2. Handgretinger R, Zugmaier G, Henze G, Kreyenberg H, Lang P and von Stackelberg A. Complete remission after blinatumomab-induced donor T-cell activation in three pediatric patients with post-transplant relapsed acute lymphoblastic leukemia. Leukemia. 2011; 25:181-184.
3. Bhojwani D and Pui CH. Relapsed childhood acute lymphoblastic leukaemia. The Lancet Oncology. 2013; 14:e205-217.
4. Nguyen K, Devidas M, Cheng SC, La M, Raetz EA, Carroll WL, Winick NJ, Hunger SP, Gaynon PS, Loh ML and Children's Oncology G. Factors influencing survival after relapse from acute lymphoblastic leukemia: a Children's Oncology Group study. Leukemia. 2008; 22:2142-2150.
5. Zugmaier G, Klinger M, Schmidt M and Subklewe M. Clinical overview of anti-CD19 BiTE and ex vivo data from anti-CD33 BiTE as examples for retargeting T cells in hematologic malignancies. Molecular Immunology. 2015; 67(2 Pt A):58-66.
6. Hoffman LM and Gore L. Blinatumomab, a Bi-Specific Anti-CD19/CD3 BiTE((R)) Antibody for the Treatment of Acute Lymphoblastic Leukemia: Perspectives and Current Pediatric Applications. Frontiers in oncology. 2014; 4:63.
7. Haas C, Krinner E, Brischwein K, Hoffmann P, Lutterbuse R, Schlereth B, Kufer P and Baeuerle PA. Mode of cytotoxic action of T cell-engaging BiTE antibody MT110. Immunobiology. 2009; 214:441-453.
8. Schlegel P, Lang P, Zugmaier G, Ebinger M, Kreyenberg H, Witte KE, Feucht J, Pfeiffer M, Teltschik HM, Kyzirakos C, Feuchtinger T and Handgretinger R. Pediatric posttransplant relapsed/refractory B-precursor acute lymphoblastic leukemia shows durable remission by therapy with the T-cell engaging bispecific antibody blinatumomab. Haematologica. 2014; 99:1212-1219.
9. Topp MS, Gokbuget N, Zugmaier G, Klappers P, Stelljes M, Neumann S, Viardot A, Marks R, Diedrich H, Faul C, Reichle A, Horst HA, Bruggemann M, et al. Phase II Trial of the Anti-CD19 Bispecific T Cell-Engager Blinatumomab Shows Hematologic and Molecular Remissions in Patients With Relapsed or Refractory B-Precursor Acute Lymphoblastic Leukemia. J Clin Oncol. 2014; 32:4134-4140.
10. Topp MS, Gokbuget N, Stein AS, Zugmaier G, O'Brien S, Bargou RC, Dombret H, Fielding AK, Heffner L, Larson RA, Neumann S, Foa R, Litzow M, et al. Safety and activity of blinatumomab for adult patients with relapsed or refractory B-precursor acute lymphoblastic leukaemia: a multicentre, single-arm, phase 2 study. The Lancet Oncology. 2015; 16:57-66.
11. Zugmaier G, Gokbuget N, Klinger M, Viardot A, Stelljes M, Neumann S, Horst HA, Marks R, Faul C, Diedrich H, Reichle A, Bruggemann M, Holland C, et al. Long-term survival and T-Cell kinetics in adult patients with relapsed/refractory B-precursor acute lymphoblastic leukemia who achieved minimal residual disease response following treatment with Anti-CD19 BiTE(R) antibody construct blinatumomab. Blood. 2015; 126:2578-84.
12. Norde WJ, Hobo W, van der Voort R and Dolstra H. Coinhibitory molecules in hematologic malignancies: targets for therapeutic intervention. Blood. 2012; 120:728-736.
13. Chen L and Flies DB. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nature reviews Immunology. 2013; 13:227-242.
14. Nirschl CJ and Drake CG. Molecular pathways: coexpression of immune checkpoint molecules: signaling pathways and implications for cancer immunotherapy. Clinical cancer research. 2013; 19:4917-4924.
15. Swann JB and Smyth MJ. Immune surveillance of tumors. The Journal of clinical investigation. 2007; 117:1137-1146.
16. Black M, Barsoum IB, Truesdell P, Cotechini T, Macdonald-Goodfellow SK, Petroff M, Siemens DR, Koti M, Craig AW and Graham CH. Activation of the PD-1/PD-L1 immune checkpoint confers tumor cell chemoresistance associated with increased metastasis. Oncotarget. 2016; 7:10557-10567. doi: 10.18632/oncotarget.7235.
17. Krupka C, Kufer P, Kischel R, Zugmaier G, Lichtenegger FS, Kohnke T, Vick B, Jeremias I, Metzeler KH, Altmann T, Schneider S, Fiegl M, Spiekermann K, et al. Blockade of the PD-1/PD-L1 axis augments lysis of AML cells by the CD33/CD3 BiTE antibody construct AMG 330: reversing a T-cell-induced immune escape mechanism. Leukemia. 2016; 30:484-491.
18. McDermott DF and Atkins MB. PD-1 as a potential target in cancer therapy. Cancer medicine. 2013; 2:662-673.
19. Fan X, Quezada SA, Sepulveda MA, Sharma P and Allison JP. Engagement of the ICOS pathway markedly enhances efficacy of CTLA-4 blockade in cancer immunotherapy. The Journal of experimental medicine. 2014; 211:715-725.
20. Page DB, Postow MA, Callahan MK, Allison JP and Wolchok JD. Immune modulation in cancer with antibodies. Annual review of medicine. 2014; 65:185-202.
21. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, Leming PD, Spigel DR, Antonia SJ, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. The New England journal of medicine. 2012; 366:2443-2454.
22. Westin JR, Chu F, Zhang M, Fayad LE, Kwak LW, Fowler N, Romaguera J, Hagemeister F, Fanale M, Samaniego F, Feng L, Baladandayuthapani V, Wang Z, et al. Safety and activity of PD1 blockade by pidilizumab in combination with rituximab in patients with relapsed follicular lymphoma: a single group, open-label, phase 2 trial. The Lancet Oncology. 2014; 15:69-77.
23. Powles T, Eder JP, Fine GD, Braiteh FS, Loriot Y, Cruz C, Bellmunt J, Burris HA, Petrylak DP, Teng SL, Shen X, Boyd Z, Hegde PS, et al. MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature. 2014; 515:558-562.
24. Nagorsen D, Bargou R, Ruttinger D, Kufer P, Baeuerle PA and Zugmaier G. Immunotherapy of lymphoma and leukemia with T-cell engaging BiTE antibody blinatumomab. Leukemia & lymphoma. 2009; 50:886-891.
25. Douer D. Will novel agents for ALL finally change the natural history? Best practice & research Clinical haematology. 2014; 27:247-258.
26. Kohnke T, Krupka C, Tischer J, Knosel T and Subklewe M. Increase of PD-L1 expressing B-precursor ALL cells in a patient resistant to the CD19/CD3-bispecific T cell engager antibody blinatumomab. Journal of hematology & oncology. 2015; 8:111.
27. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, Roche PC, Lu J, Zhu G, Tamada K, Lennon VA, Celis E and Chen L. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nature medicine. 2002; 8:793-800.
28. Penaloza-MacMaster P, Kamphorst AO, Wieland A, Araki K, Iyer SS, West EE, O'Mara L, Yang S, Konieczny BT, Sharpe AH, Freeman GJ, Rudensky AY and Ahmed R. Interplay between regulatory T cells and PD-1 in modulating T cell exhaustion and viral control during chronic LCMV infection. The Journal of experimental medicine. 2014; 211:1905-1918.
29. Huang RY, Eppolito C, Lele S, Shrikant P, Matsuzaki J and Odunsi K. LAG3 and PD1 co-inhibitory molecules collaborate to limit CD8+ T cell signaling and dampen antitumor immunity in a murine ovarian cancer model. Oncotarget. 2015; 6:27359-27377. doi: 10.18632/oncotarget.4751.
30. Sakuishi K, Apetoh L, Sullivan JM, Blazar BR, Kuchroo VK and Anderson AC. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. The Journal of experimental medicine. 2010; 207:2187-2194.
31. Rathi C and Meibohm B. Clinical pharmacology of bispecific antibody constructs. Journal of clinical pharmacology. 2015; 55 Suppl 3:S21-28.
32. Klinger M, Brandl C, Zugmaier G, Hijazi Y, Bargou RC, Topp MS, Gokbuget N, Neumann S, Goebeler M, Viardot A, Stelljes M, Bruggemann M, Hoelzer D, et al. Immunopharmacologic response of patients with B-lineage acute lymphoblastic leukemia to continuous infusion of T cell-engaging CD19/CD3-bispecific BiTE antibody blinatumomab. Blood. 2012; 119:6226-6233.
33. De Rosa SC, Brenchley JM and Roederer M. Beyond six colors: a new era in flow cytometry. Nature medicine. 2003; 9:112-117.
34. Banchereau J, Bazan F, Blanchard D, Briere F, Galizzi JP, van Kooten C, Liu YJ, Rousset F and Saeland S. The CD40 antigen and its ligand. Annual review of immunology. 1994; 12:881-922.
35. Glouchkova L, Ackermann B, Zibert A, Meisel R, Siepermann M, Janka-Schaub GE, Goebel U, Troeger A and Dilloo D. The CD70/CD27 pathway is critical for stimulation of an effective cytotoxic T cell response against B cell precursor acute lymphoblastic leukemia. Journal of immunology. 2009; 182:718-725.
36. Israel BF, Gulley M, Elmore S, Ferrini S, Feng WH and Kenney SC. Anti-CD70 antibodies: a potential treatment for EBV+ CD70-expressing lymphomas. Molecular cancer therapeutics. 2005; 4:2037-2044.
37. Sica GL, Choi IH, Zhu G, Tamada K, Wang SD, Tamura H, Chapoval AI, Flies DB, Bajorath J and Chen L. B7-H4, a molecule of the B7 family, negatively regulates T cell immunity. Immunity. 2003; 18:849-861.
38. Wang XB, Zheng CY, Giscombe R and Lefvert AK. Regulation of surface and intracellular expression of CTLA-4 on human peripheral T cells. Scandinavian journal of immunology. 2001; 54:453-458.
39. Cai G and Freeman GJ. The CD160, BTLA, LIGHT/HVEM pathway: a bidirectional switch regulating T-cell activation. Immunological reviews. 2009; 229:244-258.
40. Yi KH and Chen L. Fine tuning the immune response through B7-H3 and B7-H4. Immunological reviews. 2009; 229:145-151.
41. Marafioti T, Paterson JC, Ballabio E, Chott A, Natkunam Y, Rodriguez-Justo M, Plonquet A, Rodriguez-Pinilla SM, Klapper W, Hansmann ML, Pileri SA, Isaacson PG, Stein H, et al. The inducible T-cell co-stimulator molecule is expressed on subsets of T cells and is a new marker of lymphomas of T follicular helper cell-derivation. Haematologica. 2010; 95:432-439.
42. Palma C, Binaschi M, Bigioni M, Maggi CA and Goso C. CD137 and CD137 ligand constitutively coexpressed on human T and B leukemia cells signal proliferation and survival. International journal of cancer. 2004; 108:390-398.
43. Rygiel TP and Meyaard L. CD200R signaling in tumor tolerance and inflammation: A tricky balance. Current opinion in immunology. 2012; 24:233-238.
44. Tu TC, Brown NK, Kim TJ, Wroblewska J, Yang X, Guo X, Lee SH, Kumar V, Lee KM and Fu YX. CD160 is essential for NK-mediated IFN-gamma production. The Journal of experimental medicine. 2015; 212:415-429.
45. Zhao Z, Condomines M, van der Stegen SJ, Perna F, Kloss CC, Gunset G, Plotkin J, Sadelain M. Structural Design of Engineered Costimulation Determines Tumor Rejection Kinetics and Persistence of CAR T Cells. Cancer Cell. 2015; 28:415-28. 24:233-238.
46. Brentjens RJ, Latouche JB, Santos E, Marti F, Gong MC, Lyddane C, King PD, Larson S, Weiss M, Rivière I, Sadelain M. Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15. Nat Med. 2003; 9:279-86.