Orchestrating an immune response against cancer with engineered immune cells expressing αβTCRs, CARs, and innate immune receptors: an immunological and regulatory challenge

Cancer Immunology, Immunotherapy

Volumn 64, Issue 7, 2015, Pages 893-902

  de Witte, Moniek A ^a   Kierkels, Guido J J ^a   Straetemans, Trudy ^a   Britten, Cedrik M ^b,c   Kuball, Jürgen ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Allogeneic stem cell transplantation; CIMT 2014; Gene therapy; Innate immune system; Phase I II clinical trials; Regulatory authorities

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; HYBRID PROTEIN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

ALLOGENEIC STEM CELL TRANSPLANTATION; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CELL ENGINEERING; CLINICAL TRIAL (TOPIC); DONOR LYMPHOCYTE INFUSION; EUROPE; GENETIC ENGINEERING; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INNATE IMMUNITY; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; TUMOR IMMUNITY; UNITED STATES; ADOPTIVE IMMUNOTHERAPY; ALLOTRANSPLANTATION; GENETICS; IMMUNOLOGY; NATURAL KILLER CELL; NEOPLASMS; STEM CELL TRANSPLANTATION; T LYMPHOCYTE; TRANSPLANTATION;

CELL ENGINEERING; HUMANS; IMMUNITY, INNATE; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, KIR; RECOMBINANT FUSION PROTEINS; STEM CELL TRANSPLANTATION; T-LYMPHOCYTES; TRANSPLANTATION, HOMOLOGOUS;

EID: 84933182956     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-015-1710-8     Document Type: Review

References (49)

1. Childs R, Chernoff A, Contentin N, Bahceci E, Schrump D, Leitman S et al (2000) Regression of metastatic renal-cell carcinoma after nonmyeloablative allogeneic peripheral-blood stem-cell transplantation. N Engl J Med 343:750–758
2. Restifo NP, Dudley ME, Rosenberg SA (2012) Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 12:269–281
3. Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A et al (2014) Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 371:2189–2199
4. Robert C, Thomas L, Bondarenko I, O’Day S, Weber J, Garbe C et al (2011) Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364:2517–2526
5. R. E. Hawkins, D. E. Gilham, R. Debets, Z. Eshhar, N. Taylor, H. Abken, T. N. Schumacher, and ATTACK Consortium (2010) Development of adoptive cell therapy for cancer: a clinical perspective. Hum Gene Ther 21:665–672
6. de Witte MA, Jorritsma A, Kaiser A, van den Boom MD, Dokter M, Bendle GM et al (2008) Requirements for effective antitumor responses of TCR transduced T cells. J Immunol 181:5128–5136
7. Gill S, Tasian SK, Ruella M, Shestova O, Li Y, Porter DL et al (2014) Preclinical targeting of human acute myeloid leukemia and myeloablation using chimeric antigen receptor-modified T cells. Blood 123:2343–2354
8. Morgan R, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM et al (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314:126–129
9. Porter DL, Levine BL, Kalos M, Bagg A, June CH (2011) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365:725–733
10. Scheper W, Gründer C, Straetemans T, Sebestyen Z, Kuball J (2013) Hunting for clinical translation with innate-like immune cells and their receptors. Leukemia 28:1181–1190
11. Cieri N, Mastaglio S, Oliveira G, Casucci M, Bondanza A, Bonini C (2014) Adoptive immunotherapy with genetically modified lymphocytes in allogeneic stem cell transplantation. Immunol Rev 257:165–180
12. Baron F, Labopin M, Blaise D, Lopez-Corral L, Vigouroux S, Craddock C et al (2014) Impact of in vivo T-cell depletion on outcome of AML patients in first CR given peripheral blood stem cells and reduced-intensity conditioning allo-SCT from a HLA-identical sibling donor: a report from the Acute Leukemia working party of the European group for blood and bone marrow transplantation. Bone Marrow Transplant 49:389–396
13. Pasquini MC, Devine S, Mendizabal A, Baden LR, Wingard JR, Lazarus HM et al (2012) Comparative outcomes of donor graft CD34+ selection and immune suppressive therapy as graft-versus-host disease prophylaxis for patients with acute myeloid leukemia in complete remission undergoing HLA-matched sibling allogeneic hematopoietic cell transpl. J Clin Oncol 30:3194–3201
14. Handgretinger R (2012) Negative depletion of CD3(+) and TcRαβ(+) T cells. Curr Opin Hematol 19:434–439
15. Bertaina A, Merli P, Rutella S, Pagliara D, Bernardo ME, Masetti R et al (2014) HLA-haploidentical stem cell transplantation after removal of ab—T and B cells in children with nonmalignant disorders. Blood 124:822–826
16. Scheper W, Sebestyen Z, Kuball J (2014) Cancer immunotherapy using γδT cells: dealing with diversity. Front Immunol 5:601
17. Nguyen S, Dhedin N, Vernant J-P, Kuentz M, Al Jijakli A, Rouas-Freiss N et al (2005) NK-cell reconstitution after haploidentical hematopoietic stem-cell transplantations: immaturity of NK cells and inhibitory effect of NKG2A override GvL effect. Blood 105:4135–4142
18. Slavin S, Naparstek E, Nagler A, Ackerstein A, Samuel S, Kapelushnik J, Brautbar C, Or R (1996) Allogeneic cell therapy with donor peripheral blood cells and recombinant human interleukin-2 to treat leukemia relapse after allogeneic bone marrow transplantation. Blood 87:2195–2204
19. Kolb HJ, Schattenberg A, Goldman JM, Hertenstein B, Jacobsen N, Arcese W et al (1995) Graft-versus-leukemia effect of donor lymphocyte transfusions in marrow grafted patients. Blood 86:2041–2050
20. Lokhorst HM, Schattenberg A, Cornelissen JJ, van Oers MH, Fibbe W, Russell I et al (2000) Donor lymphocyte infusions for relapsed multiple myeloma after allogeneic stem-cell transplantation: predictive factors for response and long-term outcome. J Clin Oncol 18:3031–3037
21. Eefting M, Halkes CJM, de Wreede LC, van Pelt CM, Kersting S, Marijt EWA et al (2014) Myeloablative T cell-depleted alloSCT with early sequential prophylactic donor lymphocyte infusion is an efficient and safe post-remission treatment for adult ALL. Bone Marrow Transplant 49:287–291
22. Kessels HW, Wolkers MC, van den Boom MD, van der Valk MA, Schumacher TN (2001) Immunotherapy through TCR gene transfer. Nat Immunol 2:957–961
23. Kunert A, Straetemans T, Govers C, Lamers C, Mathijssen R, Sleijfer S, Debets R (2013) TCR-engineered T cells meet new challenges to treat solid tumors: choice of antigen, T cell fitness, and sensitization of tumor Milieu. Front Immunol 4:363
24. Matsushita H, Vesely MD, Koboldt DC, Rickert CG, Uppaluri R, Magrini VJ, Arthur CD et al (2012) Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 482:400–404
25. Robbins PF, Lu YC, El-Gamil M, Li YF, Gross C, Gartner J et al (2013) Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat Med 19:747–752
26. Grupp S, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR et al (2013) Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 368:1509–1518
27. Maus MV, Grupp S, Porter DL, June CH (2014) Antibody-modified T cells: CARs take the front seat for hematologic malignancies. Blood 123:2625–2635
28. Cooper MA, Fehniger TA, Caligiuri MA (2001) The biology of human natural killer-cell subsets. Trends Immunol 22:633–640
29. Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, Spies T (1999) Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285:727–729
30. Spear P, Wu MR, Sentman ML, Sentman CL (2013) NKG2D ligands as therapeutic targets. Cancer Immun 13:8
31. Arnon TI, Markel G, Bar-Ilan A, Hanna J, Fima E, Benchetrit F et al (2008) Harnessing soluble NK cell killer receptors for the generation of novel cancer immune therapy. PLoS ONE 3:e2150
32. Ciccone E, Pende D, Viale O, Than A, Di Donato C, Orengo AM et al (1992) Involvement of HLA class I alleles in natural killer (NK) cell-specific functions: expression of HLA-Cw3 confers selective protection from lysis by alloreactive NK clones displaying a defined specificity (specificity 2). J Exp Med 176:963–971
33. Vey N, Bourhis JH, Boissel N, Bordessoule D, Prebet T, Charbonnier A et al (2012) A phase 1 trial of the anti-inhibitory KIR mAb IPH2101 for AML in complete remission. Blood 120:4317–4323
34. Zhang T, Sentman CL (2011) Cancer immunotherapy using a bispecific NK receptor fusion protein that engages both T cells and tumor cells. Cancer Res 71:2066–2076
35. D’Asaro M, La Mendola C, Di Liberto D, Orlando V, Todaro M, Spina M et al (2010) V gamma 9 V delta 2 T lymphocytes efficiently recognize and kill zoledronate-sensitized, imatinib-sensitive, and imatinib-resistant chronic myelogenous leukemia cells. J Immunol 184:3260–3268
36. Todaro M, D’Asaro M, Caccamo N, Iovino F, Francipane MG, Meraviglia S et al (2009) Efficient killing of human colon cancer stem cells by gammadelta T lymphocytes. J Immunol 182:7287–7296
37. Xiang Z, Liu Y, Zheng J, Liu M, Lv A, Gao Y et al (2014) Targeted activation of human Vγ9 Vδ2-T cells controls epstein-barr virus-induced B cell lymphoproliferative disease. Cancer Cell 26:565–576
38. Gründer C, van Dorp S, Hol S, Drent E, Straetemans T, Heijhuurs S et al (2012) γ9 and δ2CDR3 domains regulate functional avidity of T cells harboring γ9δ2TCRs. Blood 120:5153–5162
39. Nedellec S, Bonneville M, Scotet E (2010) Human Vgamma9Vdelta2 T cells: from signals to functions. Semin Immunol 22:199–206
40. Jinushi M, Hodi FS, Dranoff G (2006) Therapy-induced antibodies to MHC class I chain-related protein A antagonize immune suppression and stimulate antitumor cytotoxicity. Proc Natl Acad Sci USA 103:9190–9195
41. Marcu-Malina V, Heijhuurs S, van Buuren M, Hartkamp L, Strand S, Sebestyen Z et al (2011) Redirecting αβ T cells against cancer cells by transfer of a broadly tumor-reactive γδT-cell receptor. Blood 118:50–59
42. Park TS, Rosenberg SA, Morgan RA (2011) Treating cancer with genetically engineered T cells. Trends Biotechnol 29:550–557
43. Stone JD, Kranz DM (2013) Role of T cell receptor affinity in the efficacy and specificity of adoptive T cell therapies. Front Immunol 4:244
44. Cameron BJ, Gerry AB, Dukes J, Harper JV, Kannan V, Bianchi FC et al (2013) Identification of a Titin-derived HLA-A1-presented peptide as a cross-reactive target for engineered MAGE A3-directed T cells. Sci Transl Med 5:197
45. Bear AS, Morgan RA, Cornetta K, June CH, Binder-Scholl G, Dudley ME et al (2012) Replication-competent retroviruses in gene-modified T cells used in clinical trials: is it time to revise the testing requirements? Mol Ther 20:246–249
46. Scholler J, Brady TL, Binder-Scholl G, Hwang W-T, Plesa G, Hege KM et al (2012) Decade-long safety and function of retroviral-modified chimeric antigen receptor T cells. Sci Transl Med 4:132
47. Britten CM, Singh-Jasuja H, Flamion B, Hoos A, Huber C, Kallen K-J et al (2013) The regulatory landscape for actively personalized cancer immunotherapies. Nat Biotechnol 31:880–882
48. Gancberg D, Draghia-Akli R (2014) Gene and cell therapy funding opportunities in horizon 2020: an overview for 2014–2015. Hum Gene Ther 25:175–177
49. Kenter MJH, Cohen AF (2012) Re-engineering the European union clinical trials directive. Lancet 379:1765–1767