Natural ligands and antibody-based fusion proteins: Harnessing the immune system against cancer

Trends in Molecular Medicine

Volumn 20, Issue 2, 2014, Pages 72-82

  Vyas, Maulik ^a   Koehl, Ulrike ^b   Hallek, Michael ^a   Strandmann, Elke Pogge von ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Cancer; Immunoconstructs; Immunoligands; NK cells; Recombinant proteins; T cells

Indexed keywords

BLINATUMOMAB; CD3 ANTIGEN; CETUXIMAB; FC RECEPTOR IIA; HYBRID PROTEIN; IPILIMUMAB; LIGAND; MONOCLONAL ANTIBODY; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NATURAL KILLER CELL RECEPTOR NKG2D; RITUXIMAB; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; TRASTUZUMAB; TUMOR ANTIGEN;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; CANCER CELL; CANCER IMMUNOTHERAPY; CANCER PATIENT; CELL MEDIATED CYTOTOXICITY; CELL PROLIFERATION; CELLULAR IMMUNITY; CLINICAL TRIAL (TOPIC); COLON CANCER; COMPLEMENT DEPENDENT CYTOTOXICITY; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; INTRACELLULAR SIGNALING; MAJOR HISTOCOMPATIBILITY COMPLEX; MALIGNANT NEOPLASTIC DISEASE; NATURAL KILLER CELL; NONHODGKIN LYMPHOMA; PHASE 1 CLINICAL TRIAL (TOPIC); PROSTATE CANCER; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR MICROENVIRONMENT;

HARNESS;

CANCER; IMMUNOCONSTRUCTS; IMMUNOLIGANDS; NK CELLS; RECOMBINANT PROTEINS; T CELLS;

ANIMALS; ANTIBODIES; ANTINEOPLASTIC AGENTS; HUMANS; IMMUNE SYSTEM; KILLER CELLS, NATURAL; LIGANDS; LYMPHOCYTE ACTIVATION; NEOPLASMS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; RECEPTORS, IGG; RECEPTORS, NATURAL CYTOTOXICITY TRIGGERING; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES;

EID: 84893647702     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2013.10.006     Document Type: Review

References (82)

1. Scott A.M., et al. Antibody therapy of cancer. Nat. Rev. Cancer 2012, 12:278-287.
2. Alderson K.L., Sondel P.M. Clinical cancer therapy by NK cells via antibody-dependent cell-mediated cytotoxicity. J. Biomed. Biotechnol. 2011, 2011:379123.
3. Shuptrine C.W., et al. Monoclonal antibodies for the treatment of cancer. Semin. Cancer Biol. 2012, 22:3-13.
4. Houot R., et al. Targeting immune effector cells to promote antibody-induced cytotoxicity in cancer immunotherapy. Trends Immunol. 2011, 32:510-516.
5. Ferris R.L., et al. Tumor antigen-targeted, monoclonal antibody-based immunotherapy: clinical response, cellular immunity, and immunoescape. J. Clin. Oncol. 2010, 28:4390-4399.
6. Chames P., et al. Therapeutic antibodies: successes, limitations and hopes for the future. Br. J. Pharmacol. 2009, 157:220-233.
7. Modjtahedi H., et al. Therapeutic application of monoclonal antibodies in cancer: advances and challenges. Br. Med. Bull. 2012, 104:41-59.
8. Kubota T., et al. Engineered therapeutic antibodies with improved effector functions. Cancer Sci. 2009, 100:1566-1572.
9. Chames P., Baty D. Bispecific antibodies for cancer therapy: the light at the end of the tunnel?. mAbs 2009, 1:539-547.
10. Pranchevicius M.C., Vieira T.R. Production of recombinant immunotherapeutics for anticancer treatment: the role of bioengineering. Bioengineered 2013, 4:305-312.
11. Muller D., et al. Improved pharmacokinetics of recombinant bispecific antibody molecules by fusion to human serum albumin. J. Biol. Chem. 2007, 282:12650-12660.
12. Kontermann R.E. Strategies for extended serum half-life of protein therapeutics. Curr. Opin. Biotechnol. 2011, 22:868-876.
13. Kontermann R. Dual targeting strategies with bispecific antibodies. mAbs 2012, 4:2.
14. Topfer K., et al. Tumor evasion from T cell surveillance. J. Biomed. Biotechnol. 2011, 2011:918471.
15. Turtle C.J., et al. Engineered T cells for anti-cancer therapy. Curr. Opin. Immunol. 2012, 24:633-639.
16. Curran K.J., et al. Chimeric antigen receptors for T cell immunotherapy: current understanding and future directions. J. Gene Med. 2012, 14:405-415.
17. Gilham D.E., et al. CAR-T cells and solid tumors: tuning T cells to challenge an inveterate foe. Trends Mol. Med. 2012, 18:377-384.
18. Grupp S.A., et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N. Engl. J. Med. 2013, 368:1509-1518.
19. Kalos M., et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci. Transl. Med. 2011, 3:95ra73.
20. Linette G.P., et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 2013, 122:863-871.
21. Staerz U.D., Bevan M.J. Hybrid hybridoma producing a bispecific monoclonal antibody that can focus effector T-cell activity. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:1453-1457.
22. Baeuerle P.A., Reinhardt C. Bispecific T-cell engaging antibodies for cancer therapy. Cancer Res. 2009, 69:4941-4944.
23. Nagorsen D., et al. Blinatumomab: a historical perspective. Pharmacol. Ther. 2012, 136:334-342.
24. Haas C., et al. Mode of cytotoxic action of T cell-engaging BiTE antibody MT110. Immunobiology 2009, 214:441-453.
25. Peng L., et al. The CEA/CD3-bispecific antibody MEDI-565 (MT111) binds a nonlinear epitope in the full-length but not a short splice variant of CEA. PLoS ONE 2012, 7:e36412.
26. Kipriyanov S.M., et al. Bispecific tandem diabody for tumor therapy with improved antigen binding and pharmacokinetics. J. Mol. Biol. 1999, 293:41-56.
27. Molhoj M., et al. CD19-/CD3-bispecific antibody of the BiTE class is far superior to tandem diabody with respect to redirected tumor cell lysis. Mol. Immunol. 2007, 44:1935-1943.
28. McAleese F., Eser M. RECRUIT-TandAbs: harnessing the immune system to kill cancer cells. Future Oncol. 2012, 8:687-695.
29. Moore P.A., et al. Application of dual affinity retargeting molecules to achieve optimal redirected T-cell killing of B-cell lymphoma. Blood 2011, 117:4542-4551.
30. Levy E.M., et al. Natural killer cells in human cancer: from biological functions to clinical applications. J. Biomed. Biotechnol. 2011, 2011:676198.
31. Flanagan M.L., et al. H60/TNT-3 fusion protein activates NK cells in vitro and improves immunotherapeutic outcome in murine syngeneic tumor models. J. Immunother. 2006, 29:274-283.
32. Germain C., et al. Redirecting NK cells mediated tumor cell lysis by a new recombinant bifunctional protein. Protein Eng. Des. Sel. 2008, 21:665-672.
33. Bauer S., et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999, 285:727-729.
34. Vitale M., et al. NK-dependent DC maturation is mediated by TNFα and IFNγ released upon engagement of the NKp30 triggering receptor. Blood 2005, 106:566-571.
35. Kellner C., et al. Promoting natural killer cell functions by recombinant immunoligands mimicking an induced self phenotype. Oncoimmunology 2013, 2:e24481.
36. Esser R., et al. NK cells engineered to express a GD2-specific antigen receptor display built-in ADCC-like activity against tumour cells of neuroectodermal origin. J. Cell. Mol. Med. 2012, 16:569-581.
37. Desjarlais J.R., et al. Optimizing engagement of the immune system by anti-tumor antibodies: an engineer's perspective. Drug Discov. Today 2007, 12:898-910.
38. Ravetch J.V., Kinet J.P. Fc receptors. Annu. Rev. Immunol. 1991, 9:457-492.
39. Hartmann F., et al. Treatment of refractory Hodgkin's disease with an anti-CD16/CD30 bispecific antibody. Blood 1997, 89:2042-2047.
40. Reiners K.S., et al. Rescue of impaired NK cell activity in Hodgkin lymphoma with bispecific antibodies in vitro and in patients. Mol. Ther. 2013, 21:895-903.
41. Zocchi M.R., et al. High ERp5/ADAM10 expression in lymph node microenvironment and impaired NKG2D ligands recognition in Hodgkin lymphomas. Blood 2012, 119:1479-1489.
42. Kellner C., et al. A novel CD19-directed recombinant bispecific antibody derivative with enhanced immune effector functions for human leukemic cells. J. Immunother. 2008, 31:871-884.
43. Singer H., et al. Effective elimination of acute myeloid leukemic cells by recombinant bispecific antibody derivatives directed against CD33 and CD16. J. Immunother. 2010, 33:599-608.
44. Stein C., et al. Novel conjugates of single-chain Fv antibody fragments specific for stem cell antigen CD123 mediate potent death of acute myeloid leukaemia cells. Br. J. Haematol. 2010, 148:879-889.
45. Kugler M., et al. A recombinant trispecific single-chain Fv derivative directed against CD123 and CD33 mediates effective elimination of acute myeloid leukaemia cells by dual targeting. Br. J. Haematol. 2010, 150:574-586.
46. Schubert I., et al. A single-chain triplebody with specificity for CD19 and CD33 mediates effective lysis of mixed lineage leukemia cells by dual targeting. mAbs 2011, 3:21-30.
47. Cho H.M., et al. Delivery of NKG2D ligand using an anti-HER2 antibody-NKG2D ligand fusion protein results in an enhanced innate and adaptive antitumor response. Cancer Res. 2010, 70:10121-10130.
48. Lam R.A., et al. Regulation of self-ligands for activating natural killer cell receptors. Ann. Med. 2013, 45:384-394.
49. Raulet D.H., et al. Regulation of ligands for the NKG2D activating receptor. Annu. Rev. Immunol. 2013, 31:413-441.
50. Groh V., et al. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002, 419:734-738.
51. Pende D., et al. Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Res. 2002, 62:6178-6186.
52. Kloess S., et al. IL-2-activated haploidentical NK cells restore NKG2D-mediated NK-cell cytotoxicity in neuroblastoma patients by scavenging of plasma MICA. Eur. J. Immunol. 2010, 40:3255-3267.
53. Mailliard R.B., et al. Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J. Immunol. 2003, 171:2366-2373.
54. Zhou H., et al. DNA-based vaccines activate innate and adaptive antitumor immunity by engaging the NKG2D receptor. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:10846-10851.
55. Ishigami S., et al. Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 2000, 88:577-583.
56. Albertsson P.A., et al. NK cells and the tumour microenvironment: implications for NK-cell function and anti-tumour activity. Trends Immunol. 2003, 24:603-609.
57. Kotturi H.S., et al. Tumor cells expressing a fusion protein of MULT1 and Fas are rejected in vivo by apoptosis and NK cell activation. Gene Ther. 2008, 15:1302-1310.
58. Kotturi H.S., et al. In vitro and in vivo delivery of novel anticancer fusion protein MULT1E/FasTI via adenoviral vectors. Cancer Gene Ther. 2010, 17:164-170.
59. von Strandmann E.P., et al. A novel bispecific protein (ULBP2-BB4) targeting the NKG2D receptor on natural killer (NK) cells and CD138 activates NK cells and has potent antitumor activity against human multiple myeloma in vitro and in vivo. Blood 2006, 107:1955-1962.
60. Jachimowicz R.D., et al. Induction of in vitro and in vivo NK cell cytotoxicity using high-avidity immunoligands targeting prostate-specific membrane antigen in prostate carcinoma. Mol. Cancer Ther. 2011, 10:1036-1045.
61. Germain C., et al. MHC class I-related chain A conjugated to antitumor antibodies can sensitize tumor cells to specific lysis by natural killer cells. Clin. Cancer Res. 2005, 11:7516-7522.
62. Kellner C., et al. Fusion proteins between ligands for NKG2D and CD20-directed single-chain variable fragments sensitize lymphoma cells for natural killer cell-mediated lysis and enhance antibody-dependent cellular cytotoxicity. Leukemia 2012, 26:830-834.
63. Koch J., et al. Activating natural cytotoxicity receptors of natural killer cells in cancer and infection. Trends Immunol. 2013, 34:182-191.
64. Zompi S., Colucci F. Anatomy of a murder-signal transduction pathways leading to activation of natural killer cells. Immunol. Lett. 2005, 97:31-39.
65. Fauriat C., et al. Deficient expression of NCR in NK cells from acute myeloid leukemia: evolution during leukemia treatment and impact of leukemia cells in NCRdull phenotype induction. Blood 2007, 109:323-330.
66. Sivori S., et al. Involvement of natural cytotoxicity receptors in human natural killer cell-mediated lysis of neuroblastoma and glioblastoma cell lines. J. Neuroimmunol. 2000, 107:220-225.
67. Tallerico R., et al. Human NK cells selective targeting of colon cancer-initiating cells: a role for natural cytotoxicity receptors and MHC class I molecules. J. Immunol. 2013, 190:2381-2390.
68. Augugliaro R., et al. Selective cross-talk among natural cytotoxicity receptors in human natural killer cells. Eur. J. Immunol. 2003, 33:1235-1241.
69. - subpopulations and in vivo influence after haploidentical NK cell infusion. J. Immunother. 2010, 33:200-210.
70. Hecht M.L., et al. Natural cytotoxicity receptors NKp30, NKp44 and NKp46 bind to different heparan sulfate/heparin sequences. J. Proteome Res. 2009, 8:712-720.
71. Pogge von Strandmann E., et al. Human leukocyte antigen-B-associated transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer cells. Immunity 2007, 27:965-974.
72. Brandt C.S., et al. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J. Exp. Med. 2009, 206:1495-1503.
73. Simhadri V.R., et al. Dendritic cells release HLA-B-associated transcript-3 positive exosomes to regulate natural killer function. PLoS ONE 2008, 3:e3377.
74. Matta J., et al. Induction of B7-H6, a ligand for the natural killer cell-activating receptor NKp30, in inflammatory conditions. Blood 2013, 122:394-404.
75. Zhang T., et al. An NKp30-based chimeric antigen receptor promotes T cell effector functions and antitumor efficacy in vivo. J. Immunol. 2012, 189:2290-2299.
76. Kellner C., et al. Mimicking an induced self phenotype by coating lymphomas with the NKp30 ligand B7-H6 promotes NK cell cytotoxicity. J. Immunol. 2012, 189:5037-5046.
77. Morgado S., et al. NK cell recognition and killing of melanoma cells is controlled by multiple activating receptor-ligand interactions. J. Innate Immun. 2011, 3:365-373.
78. Deguine J., et al. Cutting edge: tumor-targeting antibodies enhance NKG2D-mediated NK cell cytotoxicity by stabilizing NK cell-tumor cell interactions. J. Immunol. 2012, 189:5493-5497.
79. Bryceson Y.T., et al. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 2006, 107:159-166.
80. Haile L.A., et al. Immune suppression: the hallmark of myeloid derived suppressor cells. Immunol. Investig. 2012, 41:581-594.
81. Oleinika K., et al. Suppression, subversion and escape: the role of regulatory T cells in cancer progression. Clin. Exp. Immunol. 2013, 171:36-45.
82. Rothe A., et al. The bispecific immunoligand ULBP2-aCEA re-directs Natural killer cells to tumor cells and reveals potent anti-tumor activity against colon carcinoma. IJC 2013, in press.